Download Auditory Brain Development in Children with Hearing Loss – Part Two

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Auditory Brain Development in
Children with Hearing Loss – Part Two
By Jace Wolfe, PhD, & Joanna Smith, MS
Editor’s Note: This is the conclusion of a two-part article. The
first part was published in the
October 2016 issue.
Horizontal sections relative to the intercommissural plane:
10 mm below
4 mm above
8 mm above
5. The secondary auditory
cortex: For sale to the highest
bidder!
Although the activity observed in
the primary auditory cortex was
certainly interesting, the most
relevant finding of the Nishimura
et al. study was the activity they
observed in the secondary au­ Figure 6. PET scan imaging results showing neural responses in the brain of a pre-­
ditory cortex (Nature. 1999; lingually deafened adult with CI after auditory deprivation since birth. Responses are
397[6715]:116). Little to no ac­ observed in a. the occipital lobe (in blue) in response to meaningless hand movetivity was observed in the sec­ ments, b. only the secondary auditory cortex (in yellow) in response to a story told
ondary auditory cortex while with sign language, and c. only in the primary auditory cortex contralateral to the imparticipants listened to running planted ear when a story is spoken while the participant used the cochlear implant for
speech, but robust neural activ­ the left ear (Reproduced with permission: Nature. 1999;397[6715]:116).
ity was observed in the area
when participants observed sign language (Fig. 6). This find­
primary auditory cortex, a functional disconnection between
ing was one of the most prominent early reports of crossthe primary and secondary cortices was postulated (Brain
modal reorganization in the secondary auditory cortices of
Res Rev. 2007;56[1]:259).
people who are born with severe to profound hearing loss
Recent research in Dr. Andrej Kral’s laboratory investigated
and deprived of access to intelligible speech during the first
activity in single neurons in the secondary auditory cortex in re­
few years of life.
sponse to cochlear implants (CIs) (J Neurosci. 2016;
Stated differently, in the absence of access to intelligible
36[23]:6175). They demonstrated that while some anatomical
speech from the primary auditory cortex, the secondary audi­
fiber tracts among cortical areas and thalamus persist in deaf­
tory cortex is colonized by the visual system to aid in visual
ness and the secondary cortex preserves some auditory respon­
function. Numerous published reports have shown similar find­
siveness, there is also an increased visual responsiveness in the
ings over the past 15 years, with some indicating activity in the
area (PLoS One. 2013;8[4]:e60093). Neurons in the secondary
secondary auditory cortex in response to tactile stimulation as
auditory area that responded to visual stimuli did not respond to
well (Brain Res Rev. 2007;56[1]:259). The acquisition of the
auditory stimuli, demonstrating that visual input occupied some
secondary auditory cortex by other sensory modalities likely ex­
of the auditory resources normally used by hearing.
plains why people who are born deaf without sufficient access
The results of Dr. Kral’s studies (along with the research of
to auditory stimuli develop exceptionally adept abilities in some
others) suggest that when the brain does not have access to
areas that involve other sensory functions (e.g., peripheral vi­
intelligible speech during the early years of life, meaningful au­
sion is better in people who are born deaf without access to
ditory input does not coordinate activity between the primary
sound during the critical period) (Trends Cogn Sci. 2006;
and secondary auditory cortices. Instead, the secondary audi­
10[11]:512). Since such reorganization occurs outside of the
tory cortex assists with other sensory functions such as visual
processing. Additionally, auditory stimulation beyond the criti­
cal period of language development finds disordered functional
Dr. Wolfe, left, is the director of
connections or interactions between the primary and second­
audiology at Hearts for Hearing
ary auditory cortices, further limiting auditory learning.
and an adjunct assistant professor at the University of Oklahoma Health Sciences Center
and Salus University. Ms. Smith,
right, is a founder and the executive director of Hearts for
Hearing in Oklahoma City.
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4. The break-up! Starring the primary and secondary
auditory cortices
At this point, a natural question to ask is, “Where does the
disconnect occur when the auditory areas of the brain do not
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receive early access to intelligible
between the primary and secondary audi­
Supragranular
speech?” To answer that question, we
tory cortices are not developed and are
1
Layers
turn to Dr. Kral’s research exploring the
pruned away in the absence of exposure
2
functions within the multiple layers of
to meaningful auditory stimulation. In­
the primary auditory cortex. The audi­
deed, visual stimulation elicits responses
tory cortex is comprised of six layers
in the secondary cortex, but it does not
3
of neurons (2-4 mm thick; Fig. 7). Affer­
promote the development of functional
Thalamic input arrives here
ent inputs from the thalamus arrive at the
synaptic connections between the pri­
cortex at layer IV, and much of the pro­
mary and secondary auditory cortices,
4
The infragranular layers of the cortex
cessing within the cortex takes place at
which are required for auditory informa­
are the output circuits of the cortex.
layers I-III (i.e. the suprgranular layers).
tion to be disseminated in a neural net­
5
Layers V-VI (i.e., the infragranular lay­
work across the brain.
ers) modulate activity in the supragran­
ular layers, serve as the output layers of
3. Kids and kittens
the cortex into the subcortical auditory
In deaf white kittens, Dr. Kral showed
6
structures, receive top-down projec­
that the loss of infragranular activity de­
Infragranular Layers
tions from higher-order areas, and in­
velopmentally occurred between four to
tegrate higher-­
order information with
five months of age. This period is consis­
the bottom-up stream of auditory input.
tent with the critical period for adaptation
Dr. Kral measured neural responses Figure 7. A visual representation of the to chronic CI stimulation (Cereb Cortex.
to auditory stimulation at the different six layers that make up the cortex
2002;12[8]:797; Brain. 2013;136[Pt 1]:­
layers of the auditory cortex using mi­ (Cereb Cortex. 2000;10[7]:714).
180-93). In other words, the critical pe­
croelectrodes inserted to varying
riod of auditory brain development
depths (Cereb Cortex. 2000;10[7]:714). Because such
spanned over the first few months of a cat’s life when cortical
testing is too invasive to conduct in young children, Dr. Kral
synapses appeared and were pruned. If auditory stimulation
completed his studies with deaf white cats. He discovered
was not provided during these first few months, during the time
activity in layers I-IV but reduced activity in layers V-VI (Fig. 8).
when synaptic development happens, development of the au­
Among other deficits, reduced infragranular layer activity in­
ditory function is severely compromised. However, if these deaf
terferes with the integration of bottom-up and top-down in­
kittens were provided with a CI within this time period (Fig. 8),
formation streams. As a result, Dr. Kral and his coauthors
the microelectrode recordings made by Dr. Kral and his col­
concluded that a functional decoupling between the primary
leagues suggest the kittens’ auditory areas of the brain devel­
and secondary auditory cortices had occurred, particularly
oped rather typically.
from the top-down information stream.
How does Dr. Kral’s research with kittens translate to kids?
This “break-up” between the primary and secondary corti­
For that answer, let’s turn to the work of Dr. Anu Sharma, who
ces has significant functional implications for auditory and
measured the latency of the P1 component of the cortical
spoken language. When auditory signals are not efficiently
auditory evoked potential (P1-CAEP) in children with normal
and effectively transmitted from the primary to secondary au­
hearing and participants who were born deaf and received a
ditory cortex, the secondary cortex cannot share spoken lan­
CI at ages ranging from about 1 year old to early adulthood
guage and other meaningful sounds with the rest of the brain.
(Ear Hear. 2002;23[6]:532). Children who received their CIs
This lack of distribution of auditory stimulation to the second­
during the first three years of life had P1 latencies that were
ary auditory cortex and then to the rest of the brain explains
similar to children with normal auditory function (Fig. 9). In
why a teenager who was born deaf and never had access to
contrast, children who received their CIs at 7 years of age or
auditory stimulation can detect sound at whisper-soft levels
older had P1 latencies that were almost invariably later than
with a CI but cannot understand conversational speech or
their age-matched peers with normal hearing. Most (but not
even distinguish between relatively disparate words. The
all) of the children who received their CIs between 4 and
bacon sizzling in the pan is audible, but the vivid experience
7 years old also had delayed P1 latencies. Dr. Sharma con­
evoked in an auditory system that has been exposed to rich
cluded that the latency of the P1 component was a biomarker
and robust auditory stimulation from birth is diminished or al­
of auditory brain development, with later latencies represent­
together absent in the brain of a child who is deprived of audi­
ing a decoupling of the primary and secondary auditory corti­
tory stimulation during the first few years of life. Auditory
ces. In short, Dr. Sharma’s P1 latencies provided an
cortex must distribute auditory stimulation to the rest of the
electrophysiologic indication of the critical period of language
brain for sounds to be endowed with higher-order meaning.
development, which has long been considered to span over
Such a connectome model of deafness has recently been used
the first two to three years of life.
to explain inter-individual variations in CI outcomes (Lancet
The functional implication of Dr. Sharma’s work is obvi­
Neurol. 2016;15[6]:610).
ous. Children with hearing loss must be appropriately fitted
Likewise, visual stimulation during the first few years of life is
with hearing technology (e.g., hearing aids or a CI) as early
not sufficient to develop, support, sustain, or lay a foundation for
as possible to avoid auditory deprivation and provide access
listening and spoken language development. Again, the underly­
to a rich and robust model of intelligible speech. Early fitting
ing explanation resides in the fact that the functional connections
of technology is necessary to feed the auditory cortex with
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adequate stimulation to promote synaptogenesis between
the primary and secondary cortices and establish the func­
tional neural networks between the secondary auditory cor­
tex and the rest of the brain to make incoming sound come
to life and possess higher-order meaning. To optimize listen­
ing and spoken language, the brain must be fed with a hearty
diet of intelligible speech. Visual stimulation does not pro­
mote the requisite connection between the primary and sec­
ondary cortices necessary to develop spoken language
skills; decades of clinical and anecdotal observations indi­
cate poor auditory and spoken language outcomes in chil­
dren who are deprived of sound during the critical period.
Also, a large number of studies show better listening, spo­
ken language, and literacy skills in children who communi­
cate using listening and spoken language relative to their
peers who use sign language or Total Communication (e.g.,
a combination of aural/oral and sign language) (Int J Audiol.
2013;52 Suppl 2:S65; Otol Neurotol. 2016;37[2]:e82; Ear
Hear. 2011;32[1 Suppl]:84S; Ear Hear. 2003;24[1 Suppl]:
121S).
We must remember that every day within the critical period
is actually critical. In other words, delays (and most probably,
lifetime deficits) in listening and spoken language abilities will
occur if a child is deprived of sound throughout the first
30 months of life, even if cochlear implantation is provided
weeks or months before the third birthday. The deprivation
that occurred during the first two and a half years of the child’s
life will almost certainly result in a weakening of the functional
synaptic connections between the primary and secondary au­
b) a subsequent decline in the functional
ditory cortices and
Naive (congenitally deaf) cat
neural networks between the secondary auditory cortex and
the rest of the brain. We know that the typical child from an
affluent home hears 46 million intelligible words by his or her
fourth birthday (American Educator, 2003). These 46 million
words serve as the bricks and mortar that lay the functional
pathways between the primary and secondary auditory corti­
ces and establish the neural networks necessary for sound to
come to life and possess higher-order meaning. Admittedly, it
is a daunting goal to provide access to these 46 million words
by the fourth birthday. To do so, we must remind ourselves
that every day within the critical period is an important oppor­
tunity to nourish the developing auditory brain with intelligible
speech.
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5 mV/mm2
500 V
5 mV/mm2
5 mV/mm2
500 V
500 V
2. Upping the ante
Important work by Mortensen and colleagues has shown that
the complex neural networks that arise when the secondary
auditory cortex shares an auditory signal with other areas of
the brain extends beyond the perspective of auditory skill de­
velopment (Neuroimage. 2006;31[2]:842). Mortensen used
PET scan to image the brain while high-performing and poorperforming CI users listened to running speech. The high per­
formers showed activity in the left inferior prefrontal cortex while
the poor performers did not (Fig. 10). The left inferior prefrontal
cortex, a region often referred to as Broca’s area, is involved
with phonological processing, phonemic awareness, speech
production, and literacy aptitude. As a result, robust connections
must be developed between the primary and secondary auditory
cortices so that the latter may facilitate responses in the left
inferior prefrontal cortex, which is imperative for several rea­
ring cat
sons. Engaging the left inferior
Cortical field potentials
Current source densities
Current source densities
prefrontal cortex in response to
a)
b)
Normal hearing cat
Naive (congenitally deaf) cat
ayer
Cortical layer
meaningful sounds is necessary
Cortical field potentials
Cortical field potentials
Current source densities
Current source densities
so that the child may learn to pro­
II
Cortical layer
Cortical layer
duce intelligible speech. As we’ve
III
known for quite some time, chil­
II
II
IV
dren speak as they hear, and ac­
III
III
IV
IV
IV
cess to intelligible words is
V/VI
IV
IV
necessary to develop intelligible
V/VI
V/VI
V/VI
speech. Furthermore, access to
V/VI
V/VI
V/VI
V/VI
V/VI
intelligible speech is necessary to
V/VI
V/VI
V/VI
develop phonemic awareness
V/VI
V/VI
V/VI
V/VI
(e.g., The “A” says “ah.”), which
V/VI
V/VI
V/VI
V/VI
V/VI
serves as the foundation for read­
ing development. To summarize,
children with hearing loss need
brain access to intelligible speech
10 20 30 40 50
10 20 30 40 50
10 20 30 40 50
10 20 30 40 50
as early and as much as possible
10 20 30 40 50
10 20 30 40 50 Time [ms] 10 20 30 40Time
50[ms]
Time [ms]
Time [ms]
to develop their auditory skills as
Time [ms]
Time [ms]
Time [ms]
Cochlear Implant
Figure
8. Single-unit neural responses to auditory stimu- well as their speech production
Cochlear Implant
lation recorded with a microelectrode inserted at differ- and literacy abilities.
ent layers within the cortex of cats. Figure 8a provides an
example of responses from normal hearing cats. Of note, 1. The auditory brain is
hungry! Feed it clearly and
robust neural responses were recorded at all six cortical
layers. Figure 8b provides an example of responses ob- frequently.
tained from a deaf white cat that received a CI after the So what do we do to promote au­
critical period of auditory brain development. Note that robust responses are only ob- ditory brain development in chil­
dren with hearing loss in order to
served in layers I through IV, a finding associated with decoupling of primary and secpromote optimization of listening,
ondary auditory cortex (Cereb Cortex. 2000;10[7]:714).
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20
P1 latency (ms)
routinely administer audiologi­
cal evaluations to ensure chil­
Age of implantation
dren are hearing well with their
350
hearing technology.
< 3.5 years
We also must make certain
3.6-6.5 years
300
that each of the child’s caregiv­
> 7 years
ers realizes the importance of
using a hearing aid, CI, and RM
250
technology during all waking
hours from the first day when
these technologies are fitted.
200
Finally, we must ­
assist the
family with creating a robust
150
daily conversational/language
model rich in intelligible speech.
Families must also be aware
100
that their child needs to hear
46 million words by the time he/
she is 4 years old and that their
50
auditory brain development de­
pends upon it. Families must
understand that a child’s long0
0 2 4 6 8 10 12 14 16 18 20 34 36
term listening, spoken language,
literacy, academic, and social
Age (years)
development is influenced by
early brain access to intelligible
speech, and they must be
Figure 9. Cortical auditory evoked potentials (CAEP)
obtained from congenitally-deafened children who re- equipped with skills to optimize
the child’s exposure to intelligi­
ceived a CI prior to 3.5 years of age (red circle), 3.6 to
ble speech. Audiologists and
6.5 years of age (blue x), and of after 7 years of age
speech-language pathologists
(black triangles). The data points are plotted relative
must work hand-in-hand with
to the 95 confidence interval lines representing typical
families to achieve these goals.
P1 CAEP latencies of children with normal hearing (Ear
Neuroscientists from around
Hear. 2002;23[6]:532).
the world have enlightened our
profession on the neurophysiologic under­
pinnings of listening and spoken language
High-comprehension
7.5
development. Of particular note, children
must have access to intelligible speech and
meaningful acoustic input to fully develop
the auditory areas of the brain and optimize
spoken language and literacy aptitude. Vi­
sual stimulation in the form of sign language
does not promote development of the func­
Activation of the LIPC requires exposure to intelligible speech.
tional synaptic connections between the
primary and secondary auditory cortices.
These connections serve as the spring­
board for a neural network/connectome
that fully engages the brain and is neces­
sary for the development of typical listening
z=5
Right hemisphere
Left hemisphere
and spoken language abilities. Modern
hearing technology (e.g., hearing aids, CIs,
High performers show activity in LIPC, while poor performers do not.
digital adaptive remote microphone sys­
tems) allows almost every child with hear­
Figure 10. PET scan imaging showing typical response of (a) high-performing
ing loss the access needed to fully develop
CI users with broad activity present in primary and secondary auditory cortex
the auditory areas of the brain. It is our job
and also in left inferior prefrontal cortex in response to auditory stimulation
from a CI, and (b) poor-performing CI users with limited activity present in pri- as pediatric hearing health care profession­
mary and secondary auditory cortex and no activity in left inferior prefrontal cor- als to provide the children we serve with the
tex in response to auditory stimulation from a CI (Neuroimage. 2006;31[2]:842). brain growth they deserve. spoken language, and literacy
abilities? We stick with the tried
and true fundamentals of mod­
ern, evidence-based pediatric
hearing health care. We seek to
accurately diagnose children
with hearing loss by 1 month of
age so that hearing aids may be
fitted using probe microphone
measures and evidence-based
targets (e.g., Desired Sensation
Level 5.0/NAL-NL2) as soon as
possible. For children with se­
vere to profound hearing loss,
we move forward with cochlear
implantation between 6 and 9
months of age. For all children
using hearing technology, we
also ensure they are fitted with
digital adaptive remote micro­
phone systems (RM) so they
have access to intelligible
speech in our noisy world. We
are convinced that the road to
46 million words is much more
manageable to navigate with
the use of a digital adaptive RM
system. Research has clearly
shown that RM technology is
the most effective means to im­
prove communication in noise
(J Am Acad Audiol. 2013;
24[8]:714; Am J Audiol. 2015;
24[3]:440). Additionally, we must
The Hearing Journal
November 2016