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Ann. N.Y. Acad. Sci. ISSN 0077-8923
ANNALS OF THE NEW YORK ACADEMY OF SCIENCES
Issue: The Neurosciences and Music IV: Learning and Memory
Auditory brain development in premature infants:
the importance of early experience
Erin McMahon,1Pia Wintermark,2and Amir Lahav1,3
1Department of Newborn Medicine, Brigham and Women’s Hospital, Boston, Massachusetts. 2Division of Newborn Medicine,
Montreal Children’s Hospital, McGill University, Montreal, Quebec, Canada. 3Department of Pediatrics, MassGeneral Hospital
for Children, Harvard Medical School, Boston, Massachusetts
Address for correspondence: Amir Lahav, ScD, PhD, The Neonatal Research Lab, Department of Newborn Medicine, 75
Francis Street, Boston, Massachusetts 02115. amir@hms.harvard.edu
Preterm infants in the neonatal intensive care unit (NICU) often close their eyes in response to bright lights, but they
cannot close their ears in response to loud sounds. The sudden transition from the womb to the overly noisy world
of the NICU increases the vulnerability of these high-risk newborns. There is a growing concern that the excess noise
typically experienced by NICU infants disrupts their growth and development, putting them at risk for hearing,
language, and cognitive disabilities. Preterm neonates are especially sensitive to noise because their auditory system
is at a critical period of neurodevelopment, and they are no longer shielded by maternal tissue. This paper discusses
the developmental milestones of the auditory system and suggests ways to enhance the quality control and type of
sounds delivered to NICU infants. We argue that positive auditory experience is essential for early brain maturation
and may be a contributing factor for healthy neurodevelopment. Further research is needed to optimize the hospital
environment for preterm newborns and to increase their potential to develop into healthy children.
Keywords: auditory; brain; prematurity; newborns; noise; plasticity
Introduction
Prematurity is the leading cause of death in the first
month of life and a major cause of long-term disabil-
ity.1Advances in neonatal care have increased the
survival rate of ailing premature newborn infants.2
However, despite these advances, premature infants
are still prone to developmental problems that may
persist throughout their lifetime.3–5 These include
deficits in hearing, attention, memory, speech, lan-
guage, social behavior, and self-regulation.6–8 Be-
cause these problems are too often seen in neonatal
intensive care unit (NICU) graduates, it is possible
that the origin of these problems may be attributed
to environmental factors, such as the acoustic envi-
ronment in the NICU. This article is not an exhaus-
tive review, but is intended to highlight the concept
that preterm newborns are at a critical period for au-
ditory development and therefore must be provided
with appropriate auditory input and careful protec-
tion against overstimulation during their prolonged
stay in the NICU. The current design of most NICUs
hasyettoachievesuchprotection.
Auditory developmental milestones
To better understand the need for auditory pro-
tection and the importance of early auditory ex-
perience, it is necessary to point out some of the
most important developmental milestones of audi-
tory development in the fetal and neonatal periods.
The development of the auditory system is an elab-
orate process that begins very early in gestation.9All
major structures of the ear, including the cochlea,
are in place between 23 and 25 weeks gestational
age (GA).9–11 Thus, unless a congenital abnormality
is present, most preterm infants can already hear
when first admitted to the NICU. The human fe-
tus can perceive and react to auditory information
starting at approximately week 26 of life.12 Begin-
ning between 26 and 30 weeks GA, hair cells in
the cochlea are fine tuned for specific frequencies
and can translate vibratory acoustic stimuli into an
doi: 10.1111/j.1749-6632.2012.06445.x
Ann. N.Y. Acad. Sci. 1252 (2012) 17–24 c
2012 New York Academy of Sciences. 17
Auditory development in preterm infants McMahon et al.
electrical signal that is sent to the brainstem.13 Be-
yond 30 weeks GA, the auditory system is mature
enough to permit complex sounds and distinguish
between different speech phonemes,10,14,15 which is
presumably the beginning of language and speech
development.16 Finally, by 35 weeks GA, auditory
processing facilitates learning and memory forma-
tion.17,18 Therefore, there is a need early on to pro-
tect preterm newborns from auditory stimuli they
are not yet ready to handle.19
Many of the sounds that are audible in the womb
are generated internally by the mother’s respira-
tion, digestion, heart rhythm, and physical move-
ments.20–22 Fetuses, however, can also respond to
sounds originated outside of the womb, such as
music and voice. These sounds stimulate the in-
ner ear through a mechanism of bone conduction.
The sound frequencies heard within the womb par-
allel the course of frequency development within
the cochlea,23 making the womb an optimal and
sheltered environment for auditory maturation. Be-
cause maternal tissue and fluid act as filters for high-
frequency sounds, the developing cochlear hair cells
are protected from potentially damaging noise.24 A
gradual exposure to low-frequency sounds first per-
mits the necessary fine tuning of the hair cells. As
the auditory system matures, it can process more
high-frequency patterns of human speech, such as
pitch, intonation, and intensity, which provide the
exogenous stimulation necessary to develop a neo-
cortical relationship with the cochlea.14 Being able
to hear these high-frequency sounds, in fact, wires
the fetus for language processing soon after it is
born.
After birth, infants seem to prefer their mother’s
voice over an unknown female voice. This has been
demonstrated in several studies showing that new-
borns selectively respond to their mother’s speech
with detectable changes in heart rate25,26 and orient-
ing movements toward27 the source of the sound.
The fact that newborn infants show a clear prefer-
ence for their mother’s voice within only hours after
birth can be taken as evidence for the significance of
prenatal hearing experience,28 suggesting that audi-
tory attention, learning, and memory begin while
in the womb.
Auditory brain plasticity
Auditory brain plasticity is intimately linked with
early sensory experience. Functions of the cerebral
cortex and the sensory systems are mostly estab-
lished during a sensitive period in the neonatal
period when neural circuitry is first generated.29
This initial neural architecture leads to different
functional areas that systematically represent dif-
ferent environmental information, and appears to
constrain further plasticity later.30 Following this
critical period, the cerebral cortex and the audi-
tory system will only be refined and reorganized
during childhood and adulthood to optimize sen-
sory processing and adaptation to environmental
changes.31
The development of the auditory cortex is heavily
dependent on the acoustic environment, as demon-
strated by both human and animal studies.30 For ex-
ample, rearing rat pups under various noise condi-
tions significantly affects the maturation time of au-
ditory cortical areas.32,33 Similarly, continuous ex-
posure to loud noise negatively affects the develop-
ment of auditory-related functions, including vocal
learning and spatial localization.34–37 These animal
studies demonstrate that changes in sensory input
can have profound effects on the functional organi-
zation of the developing cortex. Furthermore, they
implicate noise as a risk factor for abnormal sen-
sory development, and provide a basis for our con-
cerns regarding the adverse effects of NICU noise
on neonatal brain development in humans.
Deprivation of maternal sounds
Infants born prematurely spend their first weeks and
even months of life in the NICU. During this time,
they are deprived of the biological maternal sounds
they would otherwise be hearing in utero. These
sounds mainly include the low-frequency bands of
mother’s voice and the continuous, rhythmic stim-
ulation of the maternal heartbeat. Deprivation of
these sounds when the auditory system is at a crit-
ical period for development can have a profound
effect on auditory brain maturation and subsequent
speech and language acquisition.38–40
A deprived auditory cortex cannot mature nor-
mally.41 Evidence coming mainly from animal stud-
ies suggests that the functional development of the
auditory system is largely influenced by environ-
mental acoustic inputs in early life.42,43 For exam-
ple, depriving juvenile birds of normal auditory
experience delayed the emergence of topographic
brain circuitry.44 Similarly, prolonged auditory
deprivation has been shown to decrease the
18 Ann. N.Y. Acad. Sci. 1252 (2012) 17–24 c
2012 New York Academy of Sciences.
McMahon et al. Auditory development in preterm infants
expression levels of selective NMDA receptors in the
rat auditory cortex during early postnatal develop-
ment.45,46 In contrast, exposing infant rat pups to
an enriched auditory environment—either with47
or without48 music stimulation—has been shown
to enhance auditory discrimination and learning
abilities. In addition, infant rat pups raised under
sensory deafness conditions have been shown to
develop abnormal synaptic morphology in the pri-
mary auditory cortex in terms of dendrite shape,
length, and spine density.49 These studies demon-
strate a high inclination for auditory brain plasticity
in the neonatal period.
Taken together, these animal studies lend sup-
port to our concerns about the possibly harmful
auditory deprivation experienced by preterm in-
fants, even in the seemingly quiet and protected
environment of the incubator. It is, therefore, rea-
sonable to assume that the lack of sufficient oppor-
tunities to perceive maternal speech sounds during
NICU hospitalization can alter brain structure and
subsequently account for some of the hearing, lan-
guage, and attention deficits often seen in NICU
graduates.
Effects of noise exposure
Unquestionably, the type of sounds and levels of
noise typically present in the NICU are very different
from those heard in the womb.9,50 Low-frequency
placental sounds in the amniotic environment are
replaced by unpredictable noise coming from venti-
lators, cardiac monitors, infusion pumps, pagers,
and alarms.24 This accumulation of background
noise,51–53 even within the seemingly protected in-
cubator,54–56 well exceeds the recommended levels
set by the American Academy of Pediatrics.57 Thus,
the current environment available to preterm in-
fants during their hospitalization is not optimal.24
NICU noise can result in detrimental health out-
comes.58–60 Loud noise can produce unwarranted
physiological changes in heart rate,61–63 blood pres-
sure,62 respiration, and oxygenation.64,65 Noise also
appears to cause hyperalertness, increased crying,
and reduced deep sleep.66 Our recent review pa-
per on this topic67 suggests that excessive exposure
to noise during the neonatal period can negatively
affect the cardiovascular and respiratory systems,
which can increase the risk for a variety of develop-
mental problems.
Clinical implications: what we can do
There are many things that can be done to improve
the auditory environment in the NICU. Our pri-
mary target should be the quality and quantity of
sounds surrounding NICU infants in order to guar-
antee optimal conditions for their growth and de-
velopment. The two main problems that should be
addressed are the high levels of noise in the NICU
and the lack of meaningful acoustic input during a
critical time for auditory brain development. Here,
we propose a number of evidence-based suggestions
that can be implemented into routine NICU care to
potentially improve health outcomes of infants born
prematurely.
How to address the problem
of environmental noise?
Improve NICU design
The concept of individual rooms for NICU patients
is still evolving.68 However, there seems to be a
consensus among both parents69 and care givers70
that the private-room NICU design is highly pre-
ferred. A recent model suggests that the transition
from an open-bay NICU to a private-room NICU
can potentially improve developmental outcomes
through mediating factors such as developmental
care, family-centered care, parental stress, staff be-
havior, and medical practices.71,72
Modify equipment
The default volume settings on many of the NICU’s
alarm systems are often unnecessarily high. Alarm
volumes should be reduced, especially at night. Re-
ducing the volume of pagers, alarms, telephones,
and intercoms should improve overall noise pollu-
tion.73 In addition, noise-making equipment, such
as metal trashcans, should be replaced with qui-
eter alternatives. Motorized paper towel dispensers
should be cautiously avoided in spite of their poten-
tial to reduce infection rates.74
Consider a silent alarm system
Substituting audible ringtones of telephones and
pagers with a silent vibration should also be con-
sidered. In this case, monitors will text events to
all the nurses in the NICU pod through a wireless
device rather than alarming at the infant’s bedside.
Previous studies taking this approach have reported
positive results.75
Ann. N.Y. Acad. Sci. 1252 (2012) 17–24 c
2012 New York Academy of Sciences. 19
Auditory development in preterm infants McMahon et al.
Change staff behavior
It is important to educate NICU staff, including
physicians, nurses, respiratory therapists, and par-
ents, about the negative impact of noise on devel-
opmental outcomes. Increasing staff awareness can
lead to significant changes in attitude and behavior,
such as redirecting loud conversations away from
patient areas and gently closing incubator doors.
Research has shown that staff behavior alone can
have an impact on the overall noise levels in the
NICU, making it a more positive environment for
growth and development.72,76
Routinely measure noise levels
Considering the evidence regarding the negative ef-
fects of noise on neonates, it is somewhat surpris-
ing that noise levels are not routinely measured in
most NICUs. Noise level meters should be placed at
the bedside to maintain quiet and ensure compli-
ance with the recommendations set by the Amer-
ican Academy of Pediatrics.57 Periodic monitoring
of noise levels is necessary to identify new sources
ofenvironmentalnoise,aswellastoevaluatethe
efficacy of noise-reduction strategies.75
Avoid earmuffs
Whileearmuffsmayseemlikeanobviouswayto
filter noxious sounds, evidence for their effective
use in NICU infants has been rather limited.77 The
use of ear protection in the NICU may carry risks
that outweigh the benefits. The constant contact
with earmuffs may present tactile overstimulation
that the infant’s sensory system is too immature to
process.78 In addition, earmuffs actually increase the
risk for auditory deprivation by blocking the already
limited human speech sounds that are available to
the infant.
How to address the problem of auditory
deprivation?
Provide kangaroo care
Kangaroo care is a common evidence-based method
for “maternalizing” the NICU experience for
preterm infants soon after birth.79–81 During kan-
garoo care, the infant is placed in a supine position
on the mother’s (or father’s) chest to have direct
skin-to-skin contact.82 The infant can then presum-
ably hear and feel the low-frequency sounds of the
maternal voice heartbeat through the skin. Kan-
garoo care has been associated with a decreased
risk of mortality83 and has been shown to pro-
mote maternal–infant bonding.84,85 However, from
an auditory perspective, kangaroo care also pro-
vides the infant with important opportunities to
process meaningful maternal sounds that would
otherwise not be available, especially in the case of
low birth-weight infants who experience prolonged
intubation.81
Play the mother’s voice inside the
incubator/crib
Although kangaroo care is strongly encouraged, in
reality, there are times when the mother cannot be
present in the NICU or the infant is too sick to be
held outside the incubator. During those times, ex-
posing the infant to audio recordings of the mother’s
voice will benefit both the mother and the baby: it al-
lows the mother to be with her infant virtually, even
when she is not there physically, and can provide the
infant with a wide range of maternal vocalizations,
including singing lullabies, reading books, and im-
provisational speaking. This should supply the ap-
propriate language stimulation that is believed to
promote hearing, speech, and social development.
Studies have shown that preterm infants who were
exposed to an audio recording of their mother’s
voice achieved full enteral feed quicker86 and showed
meaningful changes in heart rate87 compared to
age-matched controls receiving routine care (for re-
view, see Ref. 88). While this approach has great
potential, further research is needed to determine
its optimal dose and long-term effects on child
development.
Introduce vocal music
Exposing preterm infants to vocal music, such as
lullabies, has been shown to increase oxygen satura-
tions, improve weight gain, and nonnutritive suck-
ing, and shorten overall hospital stay.89–95 Voc a l mu -
sic is comprised of a large spectrum of intonations
and vocalizations, both rhythmic and melodic,96
which can provide adequate exposure to language
stimuli when the live mother’s voice is not avail-
able.97 Vocal music, in particular, may also be bi-
ologically meaningful when sung by the mother.
Combining live singing with kangaroo care may thus
offer a perfectly viable way to warmly immerse the
infant with soothing maternal sounds.98,99 Any at-
tempt to play other forms of music, such as purely
instrumental pieces, must be taken with caution as
this type of auditory stimulation cannot properly
address the problem of maternal sound deprivation.
20 Ann. N.Y. Acad. Sci. 1252 (2012) 17–24 c
2012 New York Academy of Sciences.
McMahon et al. Auditory development in preterm infants
According to a recent review by Neal and Lindeke,100
there is still controversy about the use of music as
a developmental care strategy in the NICU, espe-
cially in infants <32 weeks GA. More controlled
and rigorous studies are needed to definitively test
the long-term effects of this therapeutic approach.
Be sensitive to the infant’s state
When providing auditory stimulation in the NICU,
whether it is vocal music or the mother’s voice, it is
critically important to pay attention to the infant’s
behavioral cues and modulate the stimulation ac-
cordingly. Preterm infants have limited capacity to
defend themselves against sensory stimulation that
is age-inappropriate with respect to duration, com-
plexity, and intensity.101 Infants will exhibit stress
signals in autonomic, motor, and self-regulatory
systems in response to irritating stimulation.102 In
accordance with the developmental care guidelines
proposed by Heidi Als,19,103 we recommend that
both parents and caregivers should develop the nec-
essary skills required to understand and respond
to the infant’s behavioral cues, and any automated
systems that provide infants with auditory stimula-
tion at a potentially inappropriate time should be
avoided.
Carefully select audio equipment
Commercially available audio equipment, such as
speakers, digital players, and cables, must be care-
fully tested for safety before it is used inside an in-
cubator or a crib as these products are not typi-
cally designed for NICU use. Testing must ensure
that the audio equipment delivers sound at a safe
decibel level for preterm newborns, does not cre-
ate electrical interference with medical equipment
such as cardiac monitors and ventilators, is resistant
against high temperature (∼36◦C) and humidity
(∼75%) levels typically present inside the incuba-
tor, and can be routinely cleaned with disinfectant
to ensure compliance with infection control regula-
tions. For a full description of recommended tests
and audio equipment, see Ref. 104.
Conclusions
The primary auditory stimulation infants receive in
the NICU is ambient noise. Thus, the prolonged
hospitalization experienced by preterm infants may
compromise development. This should no longer be
ignored or devalued. Emphasis must be placed on
making the NICU a more conducive environment
for positive auditory experience. This early auditory
experience occurs at the most critical period for
neural wiring and subsequent neurodevelopment.
Efforts should be made to envelop the preterm in-
fants with more womb-like sounds to compensate
for the loss of exposure to the maternal voice and
heartbeat and to protect them from potentially ad-
verse noise effects.
Acknowledgements
This work was supported by the following founda-
tions: Christopher Joseph Concha, Hailey’s Hope,
Capita, Waterloo, Heather on Earth, Christopher
Douglas Hidden Angel, and Peter and Elizabeth C.
Tower, as well as by the John Alden Trust, Lifespan
Healthcare, and Philips Healthcare.
Conflicts of interest
The authors declare no conflicts of interest.
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