Hearing Research 308 (2014) 27e40

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Hearing Research
journal homepage: www.elsevier.com/locate/heares

Review

Function and plasticity of the medial olivocochlear system

in musicians: A review
Xavier Perrot a, b, c, d, *, Lionel Collet a, b, c, d
a
Universit de Lyon, Lyon F-69000, France
b
INSERM U1028, CNRS UMR5292, Universit Lyon 1, Lyon Neuroscience Research Center, Brain Dynamics and Cognition Team, Lyon F-69000, France
c
Claude Bernard Lyon 1 University, Lyon F-69500, France
d
Hospices Civils de Lyon, Lyon Sud Teaching Hospital, Department of Audiology and Orofacial Explorations, Pierre-Bnite F-69310, France

a r t i c l e i n f o a b s t r a c t

Article history: The outer hair cells of the organ of Corti are the target of abundant efferent projections from the olivo-
Received 23 May 2013 cochlear system. This peripheral efferent auditory subsystem is currently thought to be modulated by
Received in revised form central activity via corticofugal descending auditory system, and to modulate active cochlear micro-
11 August 2013
mechanics. Although the function of this efferent subsystem remains unclear, physiological, psycho-
Accepted 21 August 2013
Available online 30 August 2013
physical, and modeling data suggest that it may be involved in ear protection against noise damage and
auditory perception, especially in the presence of background noise. Moreover, there is mounting evidence
that its activity is modulated by auditory and visual attention. A commonly used approach to measure
olivocochlear activity noninvasively in humans relies on the suppression of otoacoustic emissions by
contralateral noise. Previous studies have found substantial interindividual variability in this effect, and
statistical differences have been observed between professional musicians and non-musicians, with
stronger bilateral suppression effects in the former. In this paper, we review these studies and discuss
various possible interpretations for these ndings, including experience-dependent neuroplasticity. We
ask whether differences in olivocochlear function between musicians and non-musicians reect differ-
ences in peripheral auditory function or in more central factors, such as topedown attentional modulation.
This article is part of a Special Issue entitled <Music: A window into the hearing brain>.

2013 Elsevier B.V. All rights reserved.

1. Introduction concerning the inuence of musical training on peripheral auditory

Musicians e most notably professional musicians e often show
exceptional auditory abilities, especially, in perceptual tasks involving
pitch discrimination (Kishon-Rabin et al., 2001; Micheyl et al., 2006),
auditory memory (Boh et al., 2011; Parbery-Clark et al., 2011; Strait
et al., 2012), or auditory attention (Strait et al., 2010, 2013a). The neural
basis of enhanced auditory perceptual performance in musicians
compared to non-musicians is not entirely clear. Several studies have
suggested that early musical training can interact with the develop-
ment, maturation, and plasticity of the central auditory system (Ellis
et al., 2012; Herholz and Zatorre, 2012; Hyde et al., 2009; Oechslin
et al., 2013; Strait et al., 2013b). However, much less is known
* Corresponding author. Centre Hospitalier Lyon-Sud, Service dAudiologie et
Explorations Orofaciales, Pavillon Chirurgical 3A, 165, Chemin du Grand Revoyet,
F-69495 Pierre-Bnite Cedex, France. Tel.: 33 4 72 66 64 06;
fax: 33 4 78 86 33 41.
E-mail addresses: xavier.perrot@chu-lyon.fr (X. Perrot), lionel.collet@chu-lyon.fr
(L. Collet).
function. Interestingly, experimental ndings obtained during the last
twenty years or so suggest that the activity of the medial olivocochlear
system (MOCS) e an efferent neural pathway originating in the
brainstem, which projects directly onto the cochleas e is enhanced in
musicians (Brashears et al., 2003; Micheyl et al., 1995a, 1997a; Perrot
et al., 1999). These ndings may have important implications for our
understanding of the neural basis of music-related changes in audi-
tory function and processing. On the peripheral side, since the MOCS
modulates active cochlear micromechanics (ACMs), which are
involved in ne auditory sensitivity, improved frequency selectivity
and enhanced dynamic range, an increase in MOCS activity may
facilitate auditory perception, notably in competitive musical envi-
ronments. On the central side, since the MOCS is likely to be under a
topedown control of corticofugal descending auditory system
(CDAS), a stronger MOCS may be interpreted as reecting a
strengthening of corticofugal modulation, thereby open to attentional
modulation and training-induced plasticity.
In this article, we provide an overview of the main research
ndings concerning MOCS function in musicians. We then consider

0378-5955/$ e see front matter 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.heares.2013.08.010
28 X. Perrot, L. Collet / Hearing Research 308 (2014) 27e40
Abbreviations
ACMs active cochlear micromechanics
AN auditory nerve
BBN broadband noise
BM basilar membrane
CDAS corticofugal descending auditory system
CN cochlear nucleus
dB decibels
DPOAE(s) distortion-product otoacoustic emission(s)
EOAE(s) evoked otoacoustic emission(s)
IDL intensity difference limen
IHC(s) inner hair cell(s)
IN interneurons
(k)Hz (kilo)hertz
LE left ear
physiological mechanisms that may be responsible for experience-
dependent changes in MOCS function. In particular, we discuss
central and peripheral neuroplasticity hypotheses, as well as the
functional, perceptual, and cognitive consequences of MOC activity
enhancement on peripheral auditory function and central auditory
processing. To put the review into context, we start with a brief
description of the main anatomical and physiological characteris-
tics of the MOCS (for detailed reviews, see Guinan, 2006, 2011;
Robles and Delano, 2008).
2. Overview of anatomical and physiological characteristics
of medial olivocochlear system
2.1. Organization of human olivocochlear system
The olivocochlear bundle, also known as the auditory efferent
system, was initially described in the cat by Rasmussen
(Rasmussen, 1946). As the name indicates, this system originates in
the superior olivary complex (SOC), which is located in the ventral
part of the pons, and it projects bilaterally onto the cochleas via the
vestibular nerves. It involves two subsystems with distinct
anatomical and functional features: the lateral olivocochlear sys-
tem, and the medial olivocochlear (MOC) system (Warr and Guinan,
1979). Although current knowledge concerning the anatomy of
these subsystems stems primarily from experimental data in feline
and rodent animal models, post-mortem studies in humans and
comparative studies in non-human primates indicate a similar
subdivision of the human olivocochlear system in those species
(Hilbig et al., 2009; Moore, 2000). To our knowledge, the function of
lateral olivocochlear system has never been assessed in humans;
accordingly, in this review, we focus on the MOCS.
2.1.1. The medial olivocochlear system
The MOCS originates in the medial part of the SOC which, in
humans, corresponds to nuclei of the periolivary region. It is
comprised of thick myelinated nerve bers which project pre-
dominantly onto the contralateral cochlea through the crossed
olivocochlear bundle. Other bers project onto the ipsilateral co-
chlea, through the uncrossed (or direct) olivocochlear bundle. Both
types of MOC bers form synapses with outer hair cells (OHCs).
2.1.2. Interspecies differences in mammalian olivocochlear system
Two main differences in the anatomy of the olivocochlear sys-
tem between humans and other mammals have been reported.
Firstly, in humans, at least one half to two thirds of olivocochlear
MEM(R) middle-ear muscle (reex)
MOC(S) medial olivocochlear (system)
ms milliseconds
Mus musicians
Nmus non-musicians
OAE(s) otoacoustic emission(s)
OHC(s) outer hair cell(s)
RE right ear
SEA stimulus-equivalent attenuation
SFOAE(s) stimulus-frequency otoacoustic emission(s)
SL sensation level
SOAE(s) spontaneous otoacoustic emission(s)
SOC superior olivary complex
SPL sound pressure level
TDT tone decay test
TEOAE(s) transiently-evoked otoacoustic emission(s)
bers are MOC bers (Moore, 2000). Secondly, comparative studies
with monkeys suggest that the number of crossed bers in humans
is slightly higher than, or equal to, the number of uncrossed bers
(Guinan, 2006; Hilbig et al., 2009).
2.2. Physiology of medial olivocochlear system
2.2.1. Neurophysiological properties of olivocochlear bers
Most electrophysiological studies have focused on MOC bers in
small mammals (Robertson and Gummer, 1985; Warren and
Liberman, 1989). However, the main ndings of these studies
have been replicated in humans (Berlin et al., 1995; Chabert et al.,
2002; Veuillet et al., 1991). One important physiological property
of olivocochlear bers is that they are responsive to many kinds of
acoustic stimulations e e.g., tones, broadband noise or amplitude-
modulated tones e applied ipsilaterally, contralaterally or bilater-
ally. This property is the basis of the non-invasive functional
assessment of MOC system activity through the acoustic suppres-
sion of otoacoustic emissions (OAEs) (Collet et al., 1990; see Section
2.4). Moreover, olivocochlear spontaneous activity coupled with
cochlear effects of transection of the olivocochlear bundle suggest
that the MOCS may exert a basal tonic control of the cochlea
(Bonls et al., 1987; Zheng et al., 2000b; see also Subsection 4.1.2).
2.2.2. Medial olivocochlear acoustic reex
Olivocochlear bers constitute the efferent pathway of an
acoustic reex loop (Liberman and Guinan, 1998). Two kinds of
MOC acoustic reexes are described: ipsilateral and contralateral
(see Fig. 1). The ipsilateral reex e which mobilizes both crossed
afferent and efferent bers e involves the contralateral crossed
MOC bundle, whereas the contralateral reex e consisting of a
single afferent crossing e involves the ipsilateral uncrossed MOC
bundle (Guinan, 2006).
2.2.3. Olivocochlear effects on peripheral auditory system
The main neurotransmitter of MOC bers is acetylcholine. Its
synaptic release induces hyperpolarization of OHCs, resulting in
direct or indirect inhibition of OHC motilities1 (see Subsection 2.4.1;
for a review on cellular and molecular mechanisms of OHC efferent
modulation, see Russell and Lukashkin, 2008; Wersinger and Fuchs,
2011). The main consequences of MOCS activation on cochlear
1
For simplicity, in this article, the expression OHC motilities is used to refer
both to somatic electromotility and to active hair-bundle motility.
 X. Perrot, L. Collet / Hearing Research 308 (2014) 27e40
Fig. 1. Organization diagram of ipsilateral and contralateral medial olivocochlear
(MOC) reexes. Both reexes are elicited by an acoustic stimulation (shown here as a
blue note), the terms ipsilateral and contralateral referring to the side of this stim-
ulation relative to the cochlea where the MOCS acts. Afferent excitatory pathways are
shown in solid green lines, efferent inhibitory pathways in dashed red lines. The
ipsilateral reex involves the following structures: ipsilateral cochlea (in this example,
right one) e with activation of inner hair cells (IHCs) e and auditory nerve (AN) type I
bers, ipsilateral cochlear nucleus (CN) and crossing interneurons (IN), contralateral
medial superior olivary complex (SOC), crossed MOC bundle back on ipsilateral cochlea
e with inhibition of outer hair cells (OHCs). The contralateral MOC reex involves the
following structures: contralateral cochlea (in this example, right one) e with acti-
vation of IHCs e and AN bers, contralateral CN and crossing interneurons, ipsilateral
medial SOC, uncrossed MOC bundle onto ipsilateral cochlea (in this example, left one)
e with inhibition of OHCs.
mechanics are a reduction of the gain of cochlear amplication and
of sound-induced basilar-membrane (BM) motion, resulting in a
decrease in afferent auditory-nerve-ber responses to sound2
(Guinan, 2006; Robles and Delano, 2008). Importantly, the effect of
MOC activity on auditory-nerve-ber activity differs depending on
the presence of background noise (see Fig. 2). As a result, MOCS
activation may have opposite sensorineural e and possibly, percep-
tual e effects on responses to transient acoustic stimuli: a reduction
in sensitivity in quiet, and an improvement of discriminability in
continuous background noise (Chintanpalli et al., 2012; Liberman
and Guinan, 1998). This may explain discrepant ndings concern-
ing the functional role of MOCS in humans (see Section 5.2).
2.3. Corticofugal modulation of medial olivocochlear system
The CDAS can modulate the activity of subcortical and brainstem
neurons (for reviews, see Suga, 2012; Winer, 2006). Interestingly,
recent electrophysiological studies in bats have shown that this
topedown inuence extends all the way down to the cochlea,
through modulation of the MOCS and ACMs (Xiao and Suga, 2002a,
2002b).
2.3.1. Corticofugal descending auditory system
Broadly, the organization of the CDAS may be summarized as
follows: (i) the CDAS originates in the auditory cortex and forms
multiple feedback loops with the ascending auditory system3
(Rouiller, 1997); (ii) the CDAS projects mainly to the ipsilateral
side of the midbrain and the brainstem; (iii) as for ascending
auditory pathways, the inferior colliculus is an almost obligatory
synaptic relay of descending auditory pathways, whereas the
2
Other MOC effects e described as non-classic effects e may act independently
from modulation of BM motion by the cochlear amplier (Guinan, 2011). Their
underlying mechanisms may involve changes in the endocochlear potential and
complex micromechanical interactions between cochlear vibrational components.
3
Since most auditory pathways are reciprocal, the descending auditory system
reproduced the organization of the ascending auditory system, with three parallel
channels anatomically and functionally distinct e corresponding to the tonotopic,
non-tonotopic (or diffuse) and polysensory systems (Rouiller, 1997).
29
Fig. 2. Diagram of MOCS effect on auditory-nerve-ber activity according to back-
ground conditions. The four curves show different patterns of rate-versus-level func-
tion for an auditory nerve (AN) ber in response to tone bursts. In a silent background
(solid lines), MOCS acts through inhibition of AN ber responses, with a shift to higher
intensities, resulting in a decreased sensitivity to sounds (1). In a continuous noise
background (dashed lines), the dynamic range of AN ber responses is compressed,
due to increased activity at low levels (with increased response threshold, 2a) and
adaptation at high levels (with decreases saturation threshold, 2b). In that case, MOCS
activation partially restores the effective dynamic range of AN ber, by decreasing
responses to background noise (3a) and increasing the level at which saturation occurs
(3b), thereby reinstating sensitivity to transient sounds. This is called the anti-(excit-
atory) masking effect of MOCS. (Adapted from Guinan, 2006)
medial geniculate body is mainly involved in thalamo-cortico-
thalamic circuits.
It is worth noting that several studies have described descend-
ing pathways from the auditory cortex that bypass the inferior
colliculus and reach directly the cochlear nucleus and the superior
olivary complex (Schoeld and Coomes, 2006). Thus, the auditory
cortex is in a position to directly modulate both the cochlear
transduction of acoustic stimuli, through the MOCS, and the initial
stages of neural sound processing, at the level of the cochlear
nucleus.
2.3.2. Cortico-olivocochlear modulation in humans
Until recently, only indirect evidence for a cerebral inuence on
MOC activity and cochlear function in humans was available, based
mainly on assessment of contralateral suppression of OAEs (see
Subsection 2.4.2). Apart from studies on attentional modulation of
the MOCS and possible effects of auditory learning, which will be
discussed below (see Subsections 4.1.1 and 4.1.3), ndings of two
experimental studies in epileptic patients have provided further
evidence in favor of this attractive hypothesis.
The rst study reported postsurgical changes in MOC activity
after resection of temporal brain structures involved in auditory
processing, with either a decrease in the ear contralateral to the
brain surgery, or an increase in the ear ipsilateral to the surgery
(Khalfa et al., 2001a). The second study used an innovative exper-
imental procedure during presurgical functional brain mapping of
refractory epilepsy (Perrot et al., 2006). By combining evoked OAE
(EOAE) recording and electrical brain stimulation, it was shown
that stimulation of auditory cortex induced a contralateral decrease
in EOAE amplitude, whereas no change occurred under stimulation
of non-auditory areas. These ndings are of utmost importance
since they provide a direct evidence of a functional cortico-
olivocochlear pathway in humans, originating in the auditory cor-
tex and modulating contralateral ACMs, via the MOCS.
30 X. Perrot, L. Collet / Hearing Research 308 (2014) 27e40
Moreover, data in normal hearing subjects have shown a func-
tional interaural asymmetry of MOC activity according to handedness,
with a stronger inhibitory effect in right ear for right-handed subjects
(Khalfa et al., 1998b). This peripheral auditory lateralization may
reect the well-known cerebral hemispheric asymmetry, particularly
for speech processing (Lazard et al., 2012), and its asymmetrical cor-
ticofugal descending inuence on MOCS (Sininger and Cone-Wesson,
2004). Besides, a reverse pattern of MOCS lateralization has been
observed in neuropsychiatric diseases such as autism and schizo-
phrenia, which may be related to abnormal brain asymmetry in these
patients (Khalfa et al., 2001b; Veuillet et al., 2001).
2.4. Assessment of medial olivocochlear system through
suppression of otoacoustic emissions
Based on cellular characteristics of OHCs and neurophysiological
properties of MOCS, Collet and colleagues developed a non-
invasive test for exploring MOC activity in humans, through
acoustic suppression of OAEs (Collet et al., 1990).
2.4.1. What are otoacoustic emissions?
2.4.1.1. General description. OAEs may be described as acoustic vi-
brations emitted by the inner ear, which go backward through the
middle ear and are recordable into the outer ear canal (for a general
review on OAEs, see Kemp, 2002). Among the four types of OAEs
conventionally described according to the measurement method,
the two most common are transiently-EOAEs (TEOAEs) e induced
by transient acoustic stimulations such as clicks or tone pips4 e and
distortion-product OAEs (DPOAEs) e which are combination tones
arising in response to continuous stimulation by two pure tones.5
2.4.1.2. Generation mechanisms of otoacoustic emissions. OAEs are
commonly regarded as by-products of vibrations induced by OHC
motilities, which are the cellular substratum of ACMs.6 In mam-
mals, two types of OHC motility have been described: (i) a somatic
electromotility, mediated by prestin e a voltage-sensitive protein
located in the lateral wall; (ii) an active hair-bundle motility,
dependent on myosin-based adaptation and Ca2-mechano-
transducer channels, with an important role of stereocilin e a
protein involved in the joint between the stereocilia (for a recent
composite review on cochlear amplication mechanisms, see
Ashmore et al., 2010).7
However, the notion that OAEs are generated through ACMs only
(Knight and Kemp, 2001) has been challenged. By analyzing phase
shifts of SFOAEs and DPOAEs according to the frequency of the
evoking stimulus components, Shera and Guinan evidenced that
OAEs were generated by two distinct e although not exclusive e
mechanisms (for a recent review, see Shera, 2004). The rst one is a
passive linear coherent reection e formerly known as place-xed
emission source, which originates in pre-existing irregularities (re-
ectors) in the cochlear partition: this mechanism is predominant
for TEOAES and SFOAEs. The second one is an active nonlinear
distortion e formerly known as wave-xed emission source, which
arises from OHC nonlinearity inherent in ACMs: this mechanism is
predominant for DPOAEs. It is worth noting that under usual
4
For a detailed guide on TEOAE recording, see Kemp et al., 1990.
5
The two other types of OAEs are stimulus-frequency otoacoustic emissions
(SFOAEs) e evoked by a single pure tone e and spontaneous otoacoustic emissions
(SOAEs) e emitted in absence of any acoustic stimulation.
6
Schematically, ACMs are characterized by four properties: amplication, fre-
quency selectivity, nonlinear compression and OAEs (Manley, 2000).
7
The respective roles of these two types of cellular processes in ACMs remain a
matter of debate, even though a combination of the two processes in an integrated
system is the most likely hypothesis (Peng and Ricci, 2011).
recording conditions, OAEs presumably reect a mixture of the two
mechanisms.
2.4.2. Principles of otoacoustic emission suppression
The method used for assessing MOC activity in humans is
applicable to all types of OAEs. In broad outline, the procedure
consists in recording OAEs in the absence and in the presence of an
acoustic stimulation, usually a broadband noise (BBN).
The most widely used technique is known as contralateral sup-
pression (or attenuation) of click-EOAEs (Berlin et al., 1993; Collet
et al., 1992). It involves two types of acoustic stimulation: ipsilateral
repetitive clicks e as evoking (or elicitor) stimulation e for recording
EOAEs in one ear; and contralateral continuous BBN e as suppressor
stimulation e applied in the other ear. BBN activates the contralateral
MOC reex (see Subsection 2.2.2 and Fig. 1), which in turn inhibits
OHC motilities and modulates generators of OAEs, thereby leading to a
decrease in OAE amplitude (see also Subsection 2.2.3 and above). The
inhibitory efferent effect is computed as the difference in EOAE
amplitude with and without contralateral noise (for more detail, see
Khalfa et al., 1998a; Veuillet et al., 1991; and Table 1, note b). In this
context, the magnitude of the contralateral suppression effect is taken
as an indication of the strength of stimulus-induced MOC activity.
Interestingly, efferent suppression can be observed even for low
sound level of contralateral noise (from 50 dB SPL).
Other methods for assessing MOC activity include the use of
ipsilateral or binaural BBN elicitors e for ipsilateral or binaural
suppression of EOAEs, as well as intermittent BBN elicitors e during
an OAE forward-masking paradigm (for more detail, see Berlin
et al., 1995 and Table 1, note k).
It is important to note that large interindividual differences in
contralateral suppression of OAEs e i.e., in MOC activity e have
been observed. This nding, possibly originating from innate bio-
logical factors, suggests that whatever its function, MOCES will not
be equally effective across individuals (Backus and Guinan, 2007;
Collet et al., 1992; de Boer and Thornton, 2008).
3. Medial olivocochlear activity in musicians
Almost fteen years ago, it has been shown that professional
musicians had a larger bilateral olivocochlear efferent suppression
than non-musicians (Perrot et al., 1999). These results, indicating a
stronger MOC activity in musicians than in non-musicians, suggest
a possible neurophysiological mechanism underlying music-
related changes in the auditory system. An interesting question,
the answer to which remains unclear, is whether this peripheral
effect reects training-induced changes in central auditory func-
tion, e.g., strengthening of corticofugal connections (see Subsection
2.3.2 and Section 4.1). Another interesting question, which also
remains open, relates to perceptual consequences of the enhanced
MOC activity in musicians, in particular, with regards to selective-
listening abilities (see Subsection 2.2.3 and Sections 5.2 and 5.3).
A caveat stems from the fact that studies of MOC activity in
musicians remain scarce. On the whole, the assessment of intergroup
differences addressed two main parameters: strength and interaural
asymmetry. It is worth noting that all of the musician participants
were either high-level music students or professional classical mu-
sicians, with a formal musical training of more than 10 years and a
daily practice of more than 3 h. Moreover, all but one of them were
instrumentalists (for detailed comparative ndings, see Table 1).
3.1. Strength of efferent suppression
Several studies have found that efferent suppression was stronger
in musicians than in non-musicians, for both right (Micheyl et al.,
1995a, 1997a) and left (Brashears et al., 2003; Perrot et al., 1999)
 X. Perrot, L. Collet / Hearing Research 308 (2014) 27e40 31

Table 1
Medial olivocochlear system activity in musicians compared to non-musicians: physiological and perceptual data.

Studies Subjects Methods Main results

A/Micheyl, 11 music students from the 1. Loudness adaptation: TDT in RE 1. TDT:

Carbonnel national music conservatory - mean adaptation levels at 4 kHz smaller in Mus
and Collet, of Lyon, France (7 females, 4 males)a - test frequencies: 0.5, 1 than in Nmus (differences controlled for sex)
1995a 24 Nmus (11 females, 13 males) and 4 kHz 2. Contralateral suppression in RE:
2. MOC activity: contralateral - stronger in Mus than in Nmus (only for 62
suppression of TEOAEs in RE and 65-dB SPL ipsilateral stimulus intensities)
(Lyon procedure of stimulus- 3. Correlation analysis:
equivalent attenuationb) - no correlation between TDT and SEA
- MOC activity explains 53% of the variance of
TDT in Mus (only 6% in Nmus)

B/Micheyl, 16 music students from the MOC activity: contralateral 1. Intragroup comparisons:
Khalfa, national music conservatory of suppression of TEOAEs in RE - in both groups: signicant decrease in TEOAE
Perrot and Lyon, France (8 females, 8 males)c (Lyon procedure of SEA) amplitude under contralateral BBN
Collet, 1997a 16 Nmus (8 females, 8 males) - for Nmus: no difference in TEOAE growth-
function parametersd (y-intercept and slope
coefcient) under contralateral BBN
- for Mus: change in TEOAE growthefunction
parameters under contralateral BBN
2. Intergroup comparisons:
- no difference for TEOAE growthefunction
parameters
- greater RE SEA of TEOAEs in Mus

C/Micheyl, 20 music students from the 1. Auditory intensity discrimination: 1. IDL:

Perrot and national music conservatory of IDL in RE
Collet, Lyon, France (10 females, 10 males)e - test tone: 1-kHz tone pip
1997b - 2I-2AFC procedure
- four conditions: quiet, ipsilateral
noise, contralateral noise,
bilateral uncorrelated noise
2. MOC activity: contralateral
suppression of TEOAEs in
RE (Lyon procedure of SEA)
- no difference between IDL in quiet and IDL
with contralateral noise
- average IDL decreased under bilateral
noise (IDL-shift)
2. Contralateral suppression in RE:
- change in TEOAE growthefunction
parameters under contralateral BBN
(with a large intersubject variability)
3. Correlation analysis:
- no correlation between normalized IDL-
shift and SEA
- positive correlation between normalized
IDL-shift and change in TEOAE growthe
function parameters

D/Perrot, 16 professional Mus or music
Micheyl, Khalfa students from national music
and Collet, 1999 conservatory of Lyon, France
(8 females, 8 males/13 right
handers, 1 ambidextrous, 2
left handers)f
16 Nmus (8 females, 8 males/
all right handers)
MOC activity: contralateral suppression
of TEOAEs in RE and LE
(Lyon procedure of SEA)
1. Intragroup comparisons:
- in both groups/both ears: signicant decrease
in TEOAE amplitude under contralateral BBN
- in both groups/both ears: change in TEOAE
growthefunction parameters under
contralateral BBNg
- in both groups: RE SEA larger than LE SEA
(stronger contralateral suppression in RE)
2. Intergroup comparisons:
- no difference in baseline TEOAE amplitude
- for both ears: change in TEOAE growthe
function parameters under contralateral BBN
larger in Musg
- for both ears: SEA was larger in Mus
- no difference in attenuation quotienth (same
interaural asymmetry of contralateral
suppression)
- for all measurements/in both ears: greater
intersubject variability in Musg
3. Correlation analysis:
- in both groups/both ears: no correlation
between baseline TEOAE amplitude and SEA
- in both groups: no correlation between
laterality quotienti and interaural asymmetry
index (attenuation quotient)g

(continued on next page)

32 X. Perrot, L. Collet / Hearing Research 308 (2014) 27e40

Table 1 (continued )

Studies Subjects Methods Main results

E/Brashears, 29 professional Mus from the 1. MEMR: ipsilateral and contralateral 1. Baseline intergroup comparisons:
Morlet, Louisiana philharmonic thresholds (0.5, 1, 2 and 4-kHz - no difference in baseline TEOAE amplitude
Berlin orchestra, USA (17 females, tones; BBN) - MEMR thresholds higher in Mus (esp. for
and Hood, 2003 12 males)j 2. MOC activity: binaural suppression contralateral 500 Hz tones)
28 Nmus (17 females, 11 males) of TEOAEs in RE and LE (Kresge 2. Bilateral binaural suppression:
Hearing Research Laboratory - global comparison: nearly signicant greater
procedurek) overall suppression (between 8 and 18 ms)
in Mus
- temporal comparison: greater late suppression
(between 8 and 20 ms) in Mus, for both ears
(signicant only for RE), with a nearly
signicant RE advantage (only for Mus)
- spectral comparison: greater suppression in
Mus, both for RE (between 1 and 4 kHz) and
LE (between 0.5 and 3.5 kHz)
- age effect: greater suppression in younger
than older subjects, for both ears (in Mus only)
- no signicant gender effect, in either group
and for either ear (trend to greater overall
suppression in women)
3. Correlation analysis: In both groups/both ears:
absence of correlation between binaural
suppression and:
- MEMR thresholds for BBN
- baseline TEOAE amplitude

This table summarizes the comparative data obtained in normal-hearing adult non-musicians (Nmus) and musicians (Mus), with studies presented in ascending
chronological order.
a
Brass and percussion instrumentalists were not included in the Mus group. There was no signicant age difference between groups (handedness not controlled).
b
Insofar as EOAE amplitude increases with ipsilateral click intensity, the Lyon procedure consisted in measuring amplitude of TEOAEs for 3 to 6 ipsilateral click
intensities (ranging from 56 to 80 dB SPL), without and with a contralateral continuous BBN (of 30 or 35 dB SL). The contralateral suppression was then computed
through the stimulus-equivalent attenuation (SEA) of TEOAEs, dened as the mean reduction across all tested ipsilateral click intensities which would be required to
obtain in silent background (i.e., without activation of MOCS) the same attenuation in TEOAE amplitude as that induced by contralateral BBN. The time window
analysis was [2.5e20 ms].
c
The Mus group included 12 string and 4 woodwind instrumentalists. Experimental groups were paired for age and sex (handedness not controlled).
d
The input/output linear growth function represents EOAE amplitude plotted against ipsilateral click intensity. It provides a comprehensive measure of MOCS
effect, regardless of click intensity, through change in function parameters (i.e., increase in slope coefcient and decrease in y-intercept).
e
The Mus group included 12 string and 6 woodwind instrumentalists, and 2 pianists (handedness not controlled).
f
The Mus group included 10 string instrumentalists, 1 utist, 4 pianists, and 1 singer. Experimental groups were paired for age and sex.
g
These are unpublished data.
h
The attenuation quotient was computed as the ratio of interaural algebraic difference of SEA relative to absolute value of the sum of the SEA:
(RE SEA  LE SEA)/jRE SEA LE SEAj.
i
The laterality quotient was assessed using a French version of the Edinburgh Handedness Inventory (Oldeld, 1971).
j
The Mus group included string, woodwind, brass and percussion instrumentalists. Experimental groups were paired for age and sex (handedness not controlled).
k
The Kresge Hearing Research Laboratory procedure is based on a forward masking paradigm: it consisted in measuring amplitude of transiently-evoked
otoacoustic emissions without and with bilateral bursts of broadband noise (at 70 dB SPL) starting 10 ms before each ipsilateral click (at 65 dB SPL). The bilateral
suppression was computed as the TEOAE root mean square amplitude difference between the sums of with-noise and without-noise conditions (two recordings for
each condition). The time and frequency window analyses were [2e20 ms] and [0.195e6.25 kHz]. Abbreviations: IDL, intensity difference limen; LE, left ear; RE,
right ear; SEA, stimulus-equivalent attenuation; TDT, tone decay test. (For other abbreviations, see Abbreviation list)

ears (Fig. 3). Interestingly, this was not only true for contralateral
suppression, which involves specically the uncrossed MOC system
(Perrot et al., 1999; Table 1-D), but also for binaural suppression,
which involves the crossed MOC system as well (Brashears et al.,
2003; Table 1-E). These results show that MOCS can be activated
not only under experimental conditions, i.e., with a monaural noise
suppressor, but also under more ecological conditions closer to
musical practice, i.e., with binaural noise suppressor (see Subsection
2.4.2).
It must be emphasized that a greater interindividual variability
in OAE suppression was observed for musicians than for non-
musicians (Micheyl et al., 1997b; Perrot et al., 1999). This nding
raises the question of whether individual factors not controlled in
these studies play a role in the development of auditory-system
specicities in musicians, in particular regarding ACMs and
MOCS functioning. On the one hand, several musical factors have
already been identied as being involved in more central plas-
ticity phenomena in musicians e e.g., earliness of musical practice
and amount of training, instrument played and listening bi-
ography, possession of perfect pitch, musical environment at
home (Elbert et al., 1995; Margulis et al., 2009; Schlaug et al.,
1995; Schneider et al., 2002, 2005; Strait et al., 2013a).8 Thus,
interindividual differences in these factors may partially account
for the observed intragroup variability of MOC activity in musi-
cians. On the other hand, since cognitive brain functions may also
be inuenced by musical expertise (Oechslin et al., 2013; Strait
et al., 2010, 2012, 2013a),9 we cannot exclude that interindi-
vidual differences in cognitive functioning during experiment e
e.g., involuntary attentional orienting to experimental acoustic
stimuli (Draganova et al., 2009) e may have interfered with
8
For a recent review on brain plasticity induced by musical training, see Herholz
and Zatorre (2012).
9
For a recent review on the interrelationship between music and cognitive
abilities, see Schellenberg and Weiss (2013).
 X. Perrot, L. Collet / Hearing Research 308 (2014) 27e40
Fig. 3. Intragroup and intergroup comparisons of mean contralateral EOAE suppres-
sion effects for both ears of musicians (Mus) and non-musicians (Nmus). The sup-
pression effect of MOCS activation (bar chart and left Y-axis, expressed in dB) is based
on the stimulus-equivalent attenuation metrics (for denition: see Note b in Table 1).
Suppression effects are signicantly larger: (i) in Mus than in Nmus, for both ears
(*p < 0.05); (ii) in right ear than in left ear, for both groups (*p < 0.05). Error bars
represent the standard errors of the across-subject means. The attenuation quotient
(box plots and right Y-axis) reects interaural asymmetry of contralateral efferent
suppression (for denition: see Note h in Table 1). There is no signicant difference
between Mus and Nmus. Bar lines (error bars) represent 25th, 50th, and 75th (10th
and 90th) percentiles; lower and upper dots represent mean of the data outside the
5th and the 95th percentiles. (Adapted from Perrot et al., 1999)
cortico-olivocochlear modulation of peripheral auditory func-
tioning (de Boer and Thornton, 2007, 2012; Giard et al., 1994;
Maison et al., 2001). It is worth noting that both hypotheses
concerning the origin of the increased variability are consistent
with the existence of a cortico-olivocochlear control of MOC ac-
tivity in humans, which may be modulated by attentional pro-
cesses and auditory training (see Subsection 2.3.2 and for
discussion, Section 4.1).
3.2. Interaural asymmetry of efferent suppression
The two studies that have assessed MOC activity in the right and
left ears of musicians have failed to demonstrate a clear difference
in interaural asymmetry of efferent suppression between musi-
cians and non-musicians (Brashears et al., 2003; Perrot et al., 1999).
In the rst study (Perrot et al., 1999; Table 1-D), musicians
showed a bilateral enhancement of MOC activity but with the same
right-ear predominance in contralateral efferent suppression as
already evidenced in non-musicians (Khalfa et al., 1998b). This
result suggests that the effect of musical exposure and/or practice
on MOC activity in musicians is global, rather than side-specic.
The result also suggests that corticofugal inuences do not elimi-
nate the pattern of right-ear predominance of MOC activity, even in
listeners with extensive musical training; this observation may be
of interest in the context of studies of speech processing (Lazard
et al., 2012) (see Subsection 2.3.2 and for further discussion,
Subsection 4.1.4).
In the second study (Brashears et al., 2003; Table 1-E), efferent
suppression was found to be stronger in musicians for the right ear
33
only; however, the difference in suppression between the left and
right ears failed to reach the statistical signicance threshold.10
3.3. Additional ndings
Other results pertaining to OAEs may be viewed as indirect
evidence of difference in MOCS functioning between musicians and
non-musicians.
A study in normal-hearing young adults found larger DPOAEs
in professional musicians than in non-musicians paired for age
and gender, irrespective of whether the musicians had absolute
pitch or not (Morawski et al., 1999). Since this difference was only
signicant for mid-range intensities of primary tones (below
60 dB SPL), and not for high stimulation levels, which also
generate passive reection responses from the basilar membrane
(Shera, 2004), it was interpreted as an indication of the inuence
of protracted musical training on ACMs. More speculatively, this
may also suggest a particular operation mode of MOCES in mu-
sicians, e.g., through a decrease in basal inhibitory activity of the
MOC (see Section 2.2.1).
However, it is worth noting that in the works of Perrot et al.
(1999) and Brashears et al. (2003), although baseline EOAE ampli-
tudes for both ears tended to be larger (albeit not statistically
signicantly) in professional musicians than in non-musicians, no
correlation between efferent suppression and baseline amplitude
of EOAEs was found (Table 1-D and 1-E). This outcome is in line
with earlier ndings in non-musician subjects, which showed that
the amplitude of EOAEs and the magnitude of contralateral OAE
suppression were two independent markers of peripheral auditory
functioning, the former reecting ACMs whereas the latter pre-
sumably reects MOC activity (Hood et al., 1996; Khalfa et al.,
1998a).
4. Mechanisms of enhanced MOC efferent suppression in
musicians
4.1. Central hypothesis: musical training related-plasticity of
corticofugal descending auditory system
The rst hypothesis involves a strengthening of cortico-
olivocochlear modulation of the MOCS with musical practice. For
such experience-dependent plasticity in corticofugal inuences on
the MOCS to occur, two conditions must be fullled: (i) a cortico-
fugal topedown control of the MOCS and (ii) a basal tonic activity
for the cortico-olivocochlear pathways, which are plastic and can
be modied by musical training.
4.1.1. Corticofugal descending modulation of cochlear functioning
In addition to studies in epileptic patients and ndings of
interaural asymmetry of the MOCS (see Subsection 2.3.2), the other
main line of evidence for a functional CDAS in humans relate to
attentional modulation of MOC activity and OAEs (for reviews, see
Meric and Collet, 1994; Giard et al., 2000).
4.1.1.1. Intramodal modulation: auditory selective attention.
Several studies have shown an inuence of attention in auditory
perceptual tasks, either on MOC activity-modulation of the
contralateral suppression of OAEs (de Boer and Thornton, 2007;
Maison et al., 2001) or on ACMs-change in OAEs recorded in quiet
(Giard et al., 1994). Results showed that, in a dichotic-listening
condition, when attention was directed toward the evoking
10
This could be related to experimental procedure used for assessing MOC ac-
tivity, i.e., a binaural (rather than a contralateral) BBN.
34 X. Perrot, L. Collet / Hearing Research 308 (2014) 27e40
stimuli, or toward the ear where EOAEs were being recorded,
efferent suppression was weaker (de Boer and Thornton, 2007) and
EOAE amplitude increased (Giard et al., 1994), suggesting tope
down inhibition of the MOCS by attention. On the contrary, when
attention was directed to probe tones embedded in the noise
suppressor of the opposite ear, efferent suppression was stronger
and EOAE amplitude decreased (Maison et al., 2001), suggesting a
topedown enhancement of MOCS. Similar results have been evi-
denced for active listening to speech embedded in a contralateral
BBN, with a greater suppression of click-EOAEs for both ears
compared with passive listening (Garinis et al., 2011). These nd-
ings suggest that topedown auditory attentional modulation can
have a differential interaural effect on cochlear functioning,
increasing efferent suppression in one ear when attention is
focusing on the other ear (de Boer and Thornton, 2007; de Boer
et al., 2012). However, it is important to note that the effects
observed in those studies were often quite small (and borderline
statistically signicant), with large interindividual differences in
the magnitude of the effects, and that other studies have obtained
different results (Harkrider and Bowers, 2009) or failed to show any
signicant attentional inuence on OAEs (Michie et al., 1996).11
4.1.1.2. Intermodal modulation: visual attention. Regarding cross-
modal attentional modulation of cochlear functioning, the most
commonly observed effect was a decrease in EOAE amplitudes
during visual detection task compared with no-task condition,
suggesting an enhancement of efferent suppression under visual
attention (Froehlich et al., 1993). However, other studies e using
binaural DPOAE recordings e showed an opposite effect, with
DPOAE amplitude greater during visual tasks than during an
auditory counting task (Srinivasan et al., 2012) whereas the de Boer
and Thorntons study (2007) e using contralateral suppression of
EOAEs e did not show any change during both passive and active
visual tasks.12
4.1.1.3. Global interpretation of attentional modulation. Two main
hypotheses can be suggested from these results. On the one
hand, attentional processes, subtended by cortico-olivocochlear
pathways, may induce topedown modulation of MOC activity
and act as a peripheral auditory ltering mechanism (Perrot
et al., 2006). On the other hand, the fact that attentional effects
on cochlear functioning include both a direct modulation of OAE
amplitude in quiet and indirect modulation through noise-
induced MOCS activation may indicate that CDAS can inuence
basal olivocochlear tonic activity (see Subsection 2.2.1) as well as
MOCS sensitivity in noise background (Mulders and Robertson,
2002).
However, given the negative results, additional work is needed
to clarify the extent to which, and the conditions under which,
peripheral auditory activity is modulated by attentional processes.
In this perspective, correlational studies based on the concurrent
assessment of MOC activity e or OAE amplitude changes e and
auditory perceptual performance e e.g., during a speech-in-noise
task, while monitoring attentional load e e.g., through pupillom-
etry or multimodal brain imaging, could prove instrumental in
clarifying these issues (Francis, 2012; Koelewijn et al., 2012; Lee
et al., 2014).
11
This apparent discrepancy was possibly related to methodological issues, such
as the presentation intensity level of stimuli (for more details, see Giard et al.,
2000).
12
This latter interstudy variability may arise from difference in levels of difculty
and attentional load of the visual task, as already suggested by results obtained in
chinchillas (Delano et al., 2007).
4.1.2. Basal cortico-olivary tonic activity
Several experimental data support the existence of a corticofugal
basal tonic activity regulating MOC activity, independently of any
specic brain activation. Experiments in animal models showed that
auditory cortex deactivation, either through cortical cooling or
neuropharmacological agents, such as GABAergic agonist or lido-
caine, resulted in amplitude decrease in cochlear microphonics (Len
et al., 2012; Xiao and Suga, 2002a). These results demonstrate that
blocking spontaneous activity of auditory cortex leads to a temporary
suspension of cortico-olivary tonic activity, thereby reducing MOCS
basal inhibition. Similarly, the use of barbiturate anesthesia, known
to induce cortical depression, has been shown to suspend contra-
lateral acoustic suppression of cochlear functioning, subsequently
restored through electrical stimulation of the inferior colliculus
(Mulders and Robertson, 2002).
In humans, Khalfa et al.s study in epileptic patients (2001a) has
shown that neurosurgical resections of auditory areas produced
changes in MOC activity (see Subsection 2.3.2). This is consistent
with the existence of a basal cortico-olivary tonic activity and with
the possibility that this activity has a differential inuence on
cochlear functioning: inhibitory in the contralateral ear, and facil-
itatory in the ipsilateral ear.
4.1.3. Perceptual learning and auditory training effect on MOC
system functioning
A third line of evidence relates to learning experiments. Two
studies have assessed the effects of perceptual training on MOCS
functioning, measured through contralateral suppression of EOAEs
(Veuillet et al., 2007; de Boer and Thornton, 2008).
In a study comparing dyslexic children to children with normal
reading abilities, Veuillet et al. (2007) showed that a number of
children with reading difculties also had impaired sensitivity to
phonemic contrast, concomitantly with abnormal interaural
asymmetry of MOC activity. In these dyslexic children, those who
improved the most their speech performance after a ve-week
audiovisual training on voicing contrast also showed a partial
normalization of MOCS functioning lateralization.
In another study carried out in normal hearing young adult
listeners, de Boer and Thornton (2008) showed that subjects with
the poorer initial performance on a speech-in-noise discrimination
task also had the weaker initial MOC activity. After a ve-day
auditory training period on the tested task, these initial poor
performers turned out to be good learners, in the sense that they
had improved discrimination abilities, whereas the initial good
performers but non-learners did not. Moreover, the perceptual
improvement was concomitant with a progressive increase in MOC
activity over the ve days of training, eventually reaching the same
level as for the good performer, non-learner group.
Taken together, these results suggest that topedown inuences
are involved in auditory perceptual learning, presumably through
training-induced short term plasticity of corticofugal neural path-
ways, as demonstrated in ferrets and bats (Bajo et al., 2010; Suga
and Ma, 2003). In this context, and although it is important to
note that these data were obtained in non-musician subjects, it is
conceivable that musical training facilitates the development of the
cortico-olivocochlear pathways during childhood in order to
improve peripheral sound encoding and central auditory process-
ing (Brashears et al., 2003; Hyde et al., 2009; Perrot et al., 1999;
Strait et al., 2012, 2013b).
4.1.4. Apparent discrepancy of the similar degree of interaural
asymmetry
The absence of increase in interaural asymmetry of efferent
suppression in musicians may seem at odds with the central hy-
pothesis, relative to the increased leftward brain asymmetry
 X. Perrot, L. Collet / Hearing Research 308 (2014) 27e40
commonly reported in neuroanatomical and electrophysiological
studies on music-related neuroplasticity (Keenan et al., 2001;
Schlaug et al., 1995; Schneider et al., 2002).
However, it is worth noting that experimental conditions (i.e.,
passive listening) and acoustic stimuli used for assessing MOC ac-
tivity (i.e., binaural stimulation with clicks and contralateral or
bilateral BBN) differed from both the usual listening conditions and
the auditory environment of musicians. This situation may then
have led to an unspecic bilateral activation of brain auditory areas
(Binder et al., 1995; Zatorre et al., 1994), thereby resulting in a non-
lateralized corticofugal modulation and a normal interaural pattern
of MOC activity (Perrot et al., 1999). Alternatively, we can assume
that these non-ecological conditions have actually assessed pe-
ripheral change in strength of the MOC reex rather than central
change in corticofugal modulation of MOCS. This relates with the
peripheral hypothesis described below.
4.2. Peripheral hypothesis: sound-conditioning-related plasticity of
the MOC system
The second hypothesis involves a change in the strength of the
MOC reex. In professional classical musicians, musical practice can
last up to 45 h per week (Pawlaczyk-quszczynska et al., 2013), with
an average of 30 h per week (Emmerich et al., 2008). It is
conceivable that such protracted exposure to e often loud e sounds
engages a mechanism of sound conditioning of the peripheral
auditory system, which may involve a reinforcement of the MOC
reex loop (Brashears et al., 2003).
4.2.1. Direct evidence of sound conditioning of MOC system
Several studies in rodents and cats have assessed the role of
MOCS in the protective effect of sound conditioning (see Section
5.1). Indeed, it has been shown that repeated sound exposure in-
duces a functional increase in MOC ber acoustic responsiveness
(Brown et al., 1998), which could witness to a long-term neuro-
plasticity in the superior olivary complex (Illing et al., 2000).
Through this phenomenon, the MOCS may partially mediate an
inner-ear protection against noise-induced damage (Kujawa and
Liberman, 1999; Maison et al., 2013).
4.2.2. Indirect evidence in musicians
In musicians, two specic ndings regarding MOC activity are in
favor of this peripheral hypothesis. In Micheyl et al.s study (1995a),
the fact that MOC activity e which was enhanced in musicians e
was linked with reduced loudness adaptation only in this group,
but not in non-musicians (Table 1-A), suggest a peripheral mech-
anism. In this perspective, chronic regular music exposure may
strengthen the MOC reex in musicians. Similarly, in Brashears
et al.s study (2003), higher middle-ear muscle reex (MEMR)
thresholds in musicians (Table 1-E) may be viewed as an indirect
sign of sound conditioning-related habituation, which may occur in
this peripheral acousticomotor reex, concomitantly with changes
in MOCS functioning.
4.3. Alternative hypothesis: involvement of MEM reex
The MEMR shares common features with the MOC reex
(Liberman and Guinan, 1998). Thus, the involvement of MEMR in
efferent suppression of OAEs is a long-standing hypothesis (Veuillet
et al., 1992). In non-musicians, several arguments have been put
forward against this hypothesis, at least for low-level suppressors;
these include a higher sound level needed for activation of the
MEMR and a different pattern of spectral and phase changes of
OAEs (Bki et al., 2000; Veuillet et al., 1992; Sun, 2008). In musi-
cians, since the MEMR may be modulated by descending
35
multisensory neural pathways (Huffman and Henson, 1990), it may
be argued that music-related brain plasticity has modied the
central modulation of MEMR. Experimental data obtained specif-
ically in musicians in Brashears et al.s study (2003) argue against
this hypothesis. Firstly, musicians had higher MEMR thresholds
than non-musicians; this should result in weaker contralateral
suppression of OAEs in musicians if the MEMR was responsible for
this effect. Secondly, the lack of correlation between bilateral sup-
pression of OAEs and MEMR thresholds for BBN, whatever the
group or the tested ear, is not consistent with MEMR participation
(Brashears et al., 2003).
5. Functional and perceptual consequences of enhanced MOC
efferent suppression in musicians
What may be some of the consequences of stronger MOC in-
uences onto the cochlea? Based on currently available data
concerning the role of the MOCS in hearing (Francis, 2012;
Guinan, 2011; Robles and Delano, 2008), three main effects of
enhanced MOC activity may be expected in musicians: (i) pro-
tection against acoustic trauma, (ii) improved hearing in noise or
in concurrent environment, and (iii) enhanced auditory selective
attention.
5.1. Protection against acoustic trauma
Musicians are exposed to louder sounds that non-musicians,
with longer exposure durations (Emmerich et al., 2008;
Pawlaczyk-quszczyn  ska et al., 2013). Thus, they should be at
greater risk of acoustic injury and occupational hearing loss
(McBride et al., 1992). Surprisingly, however, several studies have
failed to nd any statistical difference in hearing thresholds be-
tween musicians and non-musicians matched for age and sex
(Karlsson et al., 1983; Schmidt et al., 1994), or found better
thresholds than predicted from similar exposure to industrial noise
according to ISO standards (Obeling and Poulsen, 1999; Pawlaczyk-
Luszczynska et al., 2013; Toppila et al., 2011). Taken together, these
ndings suggest that musicians may be less vulnerable to acoustic
trauma than non-musicians. What might be the origin of this
effect?
Electrophysiological and behavioral data in animals have shown
that MOCS activation via electrical or binaural acoustic stimulation
can lead to smaller temporary threshold shifts following exposure
to loud sounds (Rajan, 2000; Rajan and Johnstone, 1988). Similarly,
smaller permanent threshold shifts were observed after sound
conditioning, concomitantly with an enhancement of MOC reex
strength (Kujawa and Liberman, 1999). Conversely, surgical cutting
of the MOC system has been found to result in larger cellular and
neuronal cochlear damage after noise exposure, and in increased
temporary and permanent threshold shifts in the de-efferented ear
(Maison et al., 2013; Zheng et al., 2000a). Moreover, the baseline
MOC reex strength can predict vulnerability of the ear to noise
damage: the stronger the MOC reex, the smaller the permanent
threshold shift13 (Maison and Liberman, 2000). It is important to
note that sound conditioning also protects efferent ber terminals
(Canlon et al., 1999), which may contribute to reinforce MOCS own
protective efciency over time, as a form of positive-feedback loop.
In addition, the MOCS has been implicated in reduction of the
detrimental effects of noise on the central auditory system from the
rst stages of development, suggesting that its protective role may
be involved and conditioned from the early years of exposure to
13
This phenomenon could underlie the interindividual variability of susceptibility
to noise.
36 X. Perrot, L. Collet / Hearing Research 308 (2014) 27e40
music (Lauer et al., 2011). Overall, these data support the view that
one function of the MOCS is to protect the inner ear, and indirectly
the central auditory system, from noise-induced damage. Together
with ndings of a reduced auditory fatigability (Micheyl et al.,
1995a; Table 1-A) and a stronger bilateral MOC activity in musi-
cians than in non-musicians (Brashears et al., 2003; Perrot et al.,
1999; Table 1-D and 1-E), they suggest a possible explanation for
the lesser noise vulnerability in musicians. However, direct evi-
dence for a link between MOC and vulnerability to acoustic damage
in musicians is lacking.
5.2. Improved hearing in noise or in concurrent environment
Musical training, especially orchestral practice, may be physio-
logically and perceptually comparable with auditory perception in
noise or in concurrent environment, so that enhanced MOC activity
may be potentially useful for music perception. As previously
described, MOCS effects on peripheral auditory system (see
Subsection 2.2.3 and Fig. 2) are likely to improve the discrimina-
bility of transient acoustic stimuli in continuous noise background
(Liberman and Guinan, 1998; Guinan, 2006).
5.2.1. Signal-in-noise perception
Various lines of electrophysiological and behavioral evidence
are consistent with an anti-masking effect of the MOCS. In partic-
ular, electrical or acoustical stimulation of MOC bers has been
found to result in enhanced representations of tones in noise in
primary afferent ber responses (Kawase et al., 1993; Winslow and
Sachs, 1987). Conversely, and consistent with the latter ndings,
surgical cutting of MOC bers has been found to result in poorer
discrimination and localization performance in noise (May and
McQuone, 1994; May et al., 2004).
In humans, the evidence for an involvement of the MOCS in
hearing in noise is less clear. Although some studies have found
statistically signicant relationships between OAE suppression and
thresholds, or performance, in tasks involving the detection or
discrimination of simple or complex signals e including speech e
in noise (e.g., de Boer and Thorton, 2008; Garinis et al., 2011; Giraud
et al., 1997; Kumar and Vanaja, 2004; Micheyl and Collet, 1996;
Micheyl et al., 1997b), others have not (e.g., Stuart and Butler,
2012; Wagner et al., 2008). Moreover, even in those studies in
which statistical relationships between OAE suppression and per-
formance in noise were observed, the direction of the relationship
was not always consistent (e.g., de Boer et al., 2012; Micheyl et al.,
1995b, 1997b). The interpretation of these results is complicated by
potential confounding factors, such as MEMR and attentional pro-
cesses. For instance, correlations between MOC activity and
listening performance could be a by-product of attention (or
arousal) inuencing both measures. Arguably, the clearest
demonstration of a link between MOC activity and sound-signal
discrimination in noise so far stems from the work of Francis and
Guinan (Francis, 2012; Francis and Guinan, 2011). In a series of
remarkably well designed experiments, these authors demon-
strated clear covariations between simultaneous behavioral and
click EOAE-amplitude measures, while subjects were engaged in a
pure-tone intensity-discrimination task in noise. Moreover, they
found that MOC activity increased when subjects attended to the
test stimuli or with task difculty, suggesting attentional processes
involvement in the enhancement of performance in noise back-
ground (see below).
In musicians, however, evidence for superior perception of
sounds in noise, compared to non-musicians, remains scarce. Two
previous studies found that professional musicians e as well as
children studying music e outperformed non-musician subjects in
various speech-in-noise tasks (Parbery-Clark et al., 2009b; Strait
et al., 2012). Interestingly, both categories of musicians have also
been found to have stronger subcortical responses to speech stimuli
in background noise than non-musicians (Parbery-Clark et al.,
2009a; Strait et al., 2012).
5.2.2. Links with attentional processes
Musical practice, especially in a musical ensemble, often re-
quires an ability to attend selectively to concurrently presented
sounds. One way to study selective attention behaviorally involves
the probe-signal method.14 Two studies using this method have
suggested that attentional processes were involved in MOC-related
enhancement of signal-in-noise perception. The rst one (Scharf
et al., 1997) found that the ability to detect tones in a continuous
noise background was impaired in the de-efferented ear of patients
in whom the vestibular nerve was sectioned. This nding was
interpreted as evidence for a benecial involvement of the MOCS in
frequency selective attention under normal conditions, i.e., in the
non-operated ear. Results of a second study (Tan et al., 2008), which
involved normal-hearing subjects, suggested that the detection of
diotically presented tones in binaural noise may be improved
through a frequency-specic attentional ltering mechanism.
5.2.3. Sound localization in noise
A recent study in normal-hearing listeners has evidenced a
signicant negative correlation between strength of MOC reex
and noise-induced degradation of performance during a tridi-
mensional sound-localization task (Andol et al., 2011). These re-
sults, which corroborate animal data (May et al., 2004), are
particularly interesting in the context of music processing. Indeed,
two brain-potential studies have shown that professional music
conductors had superior auditory processing in horizontal pe-
ripheral space, compared to professional pianists and non-
musicians, and that this perceptual advantage may be related to
attentional processes (Nager et al., 2003; Mnte et al., 2001). Taken
together, these ndings suggest that corticofugal strengthening of
MOCS may contribute to an improvement of auditory spatial
localization in musicians. The apparently contradictory lack of pe-
ripheral enhancement among pianists could be related to a usual
exposure to less spatialized environments during their piano
practice.
5.3. Enhanced auditory selective attention
As previously described, various ndings indicate attentional
modulation of both efferent suppression and OAEs (see Subsection
4.1.1), suggesting that the MOCS may be the nal link in a
descending control pathway linking the auditory cortex to the co-
chlea (Giard et al., 2000; Perrot et al., 2006; Strait et al., 2010).
However, they raise the question of the underlying mechanisms, in
particular regarding the interindividual differences observed in
attentional effects (de Boer and Thornton, 2007, 2008; de Boer
et al., 2012; Francis, 2012; Strait et al., 2010).
5.3.1. Links with training-induced efciency of MOC system
In the de Boer and Thorton learning experiment (2008),
although MOC activity measured initially was able to predict
training-induced improvement in the individual speech-in-noise
performance, there was no more correlation between MOC activ-
ity and perceptual task scores after training (see Subsection 4.1.3).
14
In this paradigm, the listener had to detect a tone at a cued frequency, in
background noise. The presentation used two kinds of stimulation: a frequent
target one at the expected frequency, and a rare deviant one at an unexpected
frequency.
 X. Perrot, L. Collet / Hearing Research 308 (2014) 27e40
These ndings suggest that subjects may or may not use a listening
strategy involving the MOCS, depending on its individual effec-
tiveness in noise background. Moreover, this MOCS-mediated
strategy could be mobilized during task adaptation, through
training-induced corticofugal attentional processes, in order to
facilitate speech-in-noise discrimination. Thus, all subjects do not
spontaneously use their MOCS for auditory processing, but may
learn to activate it through corticofugal recruiting, provided it re-
sults in a perceptual benet (de Boer et al., 2012; Guinan, 2011). The
individual prole for MOCS use, as well as interindividual differ-
ence in MOCS basic efciency, may help to explain the experi-
mental discrepancies found between previous studies (e.g., de Boer
et al., 2012; Micheyl et al., 1997b). However, one must keep in mind
that it remains unknown whether such variability is also present in
musicians.
5.3.2. Links with conditions of MOC system activation
An important inference may be drawn from the mixed results on
attentional modulation, in particular de Boer et al.s (2012) as well
as Scharf et al.s (1997) studies (see Subsection 5.2.2). It appears
that the benecial effect of MOCS activation may be evidenced even
in monaural condition during topedown attentional processes,
while it may require binaural condition for peripheral reexive
MOC involvement e both conditions being not mutually exclusive.
Recent data in normal-hearing subjects reinforce this hypothesis by
showing that speech processing abilities in silent background,
namely binaural phonemic restoration in time-reversed speech, is
correlated with a stronger MOC efferent suppression in the right
ear (Grataloup et al., 2009). In that case, the lack of noisy envi-
ronment for activating MOCS may have been made up for an in-
crease in attentional load, in order to pass the task (Delano et al.,
2007; Francis, 2012).
5.3.3. Links with cognitive abilities
Several studies in musicians e both adult professionals and
child beginners e have reported that musicians have enhanced
basic perceptual auditory abilities, such as improved pitch-
discrimination thresholds (Kishon-Rabin et al., 2001; Micheyl
et al., 2006), as well as nonmusical cognitive abilities (for a recent
review, see Schellenberg and Weiss, 2013). Recent ndings have
supplemented these data by showing a triple relationship between:
(i) cognitive abilities, notably auditory attention and working
memory; (ii) basic auditory perception; and (iii) musical experience
(Parbery-Clark et al., 2011; Strait et al., 2010, 2012). One interpre-
tation of these ndings is that protracted musical practice can
strengthen cognitive functioning, which in turn may improve
auditory skills and performance, through enhanced attention and e
possibly e enhanced corticofugal control (Oechslin et al., 2013;
Strait et al., 2010, 2013a). However, the latter hypothesis remains
untested.
6. Conclusion and perspectives
Despite the limited experimental data available for direct evi-
dence, this review clearly demonstrates that musical training and/
or exposure can strengthen MOC activity in both ears of musicians,
possibly through a reinforcement of corticofugal topedown control
(Perrot et al., 1999). Functional benets may include reinforcement
of protection against acoustic trauma, improvement of auditory
discrimination in noise, as well as enhancement of auditory
attention and training. More specically, this feature could give
musicians an auditory-perceptual advantage enabling them to
improve auditory signal processing e from peripheral transduction
to subcortical neural encoding (for reviews, see Bidelman, 2013;
Kraus and Chandrasekaran, 2010). As a consequence, this may
37
enhance the processing of musical sounds as well as complex
acoustic patterns e such as speech in noise e or auditory se-
quences, especially in competitive environments e such as in an
orchestral background (Krishnan et al., 2012).
Although the underlying neurophysiological mechanisms
remain unclear, a unifying e albeit speculative e conception would
involve both central and peripheral experience-dependent neuro-
plasticity processes: the former, related to active musical training,
should enhance CDAS topedown inuence on MOC activity and
may be subject to an attentional control; the latter, related to
passive sound conditioning, should strengthen MOC reex loop and
may be independent of any attentional modulation.
These ndings and hypotheses require further study, in order to
reveal all their potential for medical and scientic applications.
Among possible directions for future work, four important issues
should be explored. Firstly, since maladaptive brain plasticity has
already been described in professional musicians (Elbert et al.,
1998), one might wonder whether excessive strengthening e or
paradoxical weakening e of MOC activity could lead to auditory
disorders such as tinnitus, hyperacusis or even early deafness
(Chry-Croze et al., 1993). Secondly, since a stronger MOCS might
provide a developmental advantage and contribute to a greater
musicianship, an alternative hypothesis to the experience-
dependent neuroplasticity would be that this feature reects an
innate auditory predisposition to music, thereby independent of
any learning- or training-induced change (Ellis et al., 2012; Norton
et al., 2005). Thirdly, since in the reported studies, all the tested
musicians but one were classical instrumentalists, one may ask if
music-related MOCS change can also be found e stronger or lesser
e in musicians exposed to another musical environment e such as
traditional musicians e or used to process other kinds of musical
stimuli e such as speech with music, for singers (Yasui et al., 2009).
Lastly, a better understanding of music-related MOCS plasticity
might help therapists better use musical training as a remediation
tool or a rehabilitation method in pathologies such as dyslexia or
auditory processing disorders (Kraus, 2012), stroke or neurode-
generative diseases (Altenmller et al., 2009), as well as in normal
or pathological aging (Sherratt et al., 2004). In this context,
assessment of MOC activity as a predictive measure of training
benet and/or as a physiological measure of perceptual improve-
ment could prove to be of particular interest.
Acknowledgments
The authors are grateful to Christophe Micheyl and two anon-
ymous reviewers for constructive comments on an earlier version
of the manuscript.
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