Download Auditory Brain Development in Children With Hearing Loss– Part One

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Auditory Brain Development in
Children With Hearing Loss – Part One
By Jace Wolfe, PhD, & Joanna Smith, MS
Editor’s Note: This is the first installment
of a two-part article. The conclusion will
be published in the November issue.
a.
D
b.
Insula
(short gyri)
Percentral
gyrus
Central sulcus
Postcentral gyrus
r. Carol Flexer aptly puts it: It’s
Planum
temporale
all about the brain. We hear
with our brain. The ears are
Wernicke’s
just the way in. Early identifiarea
cation of hearing loss and intervention
Transverse
must occur during the critical period of
(Heschl’s) Gyrus
language development in the brain. Listening happens in the brain, not in the ears.
As pediatric hearing healthcare profesPrimary Auditory Cortex
sionals, we are familiar with these mantras
and catchphrases. In fact, we have heard
and said these slogans so much that they Figure 1a. A visual representation of the classical ascending auditory pathway
almost seem like clichés. But there are from the cochlea to primary auditory cortex. Figure 1b: Primary auditory cortex
power truths behind clichés that make (Heschl’s gyrus) identified by the red arrow (Reproduced with permission: Bhatthem stand the test of time. Too often we nagar. Neuroscience for the Study of Communicative Disorders. 2nd ed. Wolters
lose sight of the exact origins of clichés Kluwer Health, 2012).
and buzz-phrases that underlie our lives.
In this two-part article, we provide a
Percentral
a. Insula
b.
gyrus
Central sulcus
brief overview of several relevant research
(short gyri)
Postcentral gyrus
studies examining the effects of hearing
Planum
loss and audiologic intervention on auditemporale
tory brain development. This summary includes a survey of research investigating
Wernicke’s
area
auditory brain development in humans and
animals, with a focus on the work of Andrej
Transverse
(Heschl’s) Gyrus
Kral, MD, PhD, one of the most prolific
scholars in the area of early auditory brain
development. His research on deaf white Figure 2a. Secondary auditory cortex identified by red arrows. Figure 2b. Seccats has substantially advanced our un- ondary auditory cortex identified by red arrows (Brodmann’s Areas 41 [primary]
derstanding of the influence of deafness and 42 [secondary]; Bhatnagar, 2012).
and cochlear implantation on auditory
brain development. We would be remiss if we failed to ac10. The Auditory Brain
knowledge a number of other brilliant researchers from around
The auditory brain extends far beyond Heschl’s gyrus and is
the world who have contributed to this line of study (including
actually quite complex. In our auditory anatomy courses, we
but not limited to Chris Ponton, Jos Eggermont, Anu Sharma,
likely learned that auditory signals travel up the brainstem to the
David Pisoni, David Ryugo, Bob Harrison, Karen Gordon,
thalamus and the primary auditory cortex (otherwise known as
Lynne Werner, Nina Kraus, and Patricia Kuhl).
Heschl’s gyrus; Figs. 1a and 1b). Heschl’s gyrus resides within
the Sylvian fissure and courses medially from the superior temporal gyrus. Tonotopic organization is preserved throughout
Dr. Wolfe, left, is the director of
this trip, including within the primary auditory cortex; additionaudiology at Hearts for Hearing
ally, complex processing, which mediates functions—from basic
and an adjunct assistant professor at the University of Oklasimple detection to complex localization and extraction of a
homa Health Sciences Center
signal of interest from competing noise—occurs in groups of
and Salus University. Ms. Smith,
neurons at all levels of the auditory nervous system.
right, is a founder and the exFrom the primary auditory cortex, auditory signals travel to the
ecutive director of Hearts for
secondary auditory cortex, which has less defined boundaries
Hearing in ­Oklahoma City.
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and components compared with the primary auditory cortex. Figure 2a shows
an elementary example of many areas in
temporal lobe and beyond that are typically thought to comprise secondary
auditory cortex. It is well known that the
secondary auditory cortex plays a prominent role in our ability to understand
speech. For instance, in 1874, Wernicke
noted that an insult to Brodmann area
22, located in the secondary auditory
cortex (Fig. 2b), results in an inability to
understand speech.
representation or feature extraction (Allen.
IEEE Trans. on Speech and Audio Processing 1994;2[4]:567; Kral. Brain Res Rev
2007;56[1]:259; Kral. e-Neuroforum 2015;
6:21). Research has shown that infants as
young as 4 months begin to attend to the
phonemes of his/her primary language while
showing weaker responses to phonemes of
foreign languages (Dahaene-Lambertz.
Trends Neurosci 2006;29[7]:367).
Researchers have suggested that the
primary auditory cortex detects acoustic
features that an individual deems important,
and the secondary and higher-order areas
9. When all goes right, the auditory
combine these features into meaningful
Figure 3. PET scan image illustrating
brain’s areas glow bright!
representations (i.e., auditory objects; Kral.
When a person has sufficient access to a broad bilateral activation of primary Neuroscience 2013;247:117; Kral, 2007).
intelligible speech throughout the first and secondary auditory cortices while Higher-order auditory areas contain pluripfew years of life, the auditory areas of the a post-lingually deafened adult with a otent neurons that respond to multiple
brain light up like Time Square in re- left ear CI listens to running speech
modes of stimulation (e.g., a neuron that
sponse to auditory stimulation (Fig. 3). (Reproduced with permission: Green.
responds to auditory, visual, and tactile
Green et al. used positron emission Hear Res 2005;205[1-2]:184).
stimulation), possibly enabling multi-modal
tomography (PET) scan testing to imintegration. Additional research is needed
age the areas of the brain that were responsive when postto fully understand the roles of pluripotent neurons in the seclingually deafened adults listened to speech while using a
ondary auditory cortex.
cochlear implant (CI; Hear Res 2005;205[1-2]:184). To clarify, the participants had normal hearing during childhood, lost
7. I like bacon!
their hearing as adults, and received a CI after a variable
We have yet to develop a full understanding of exactly how
range of duration of deafness (1 to 48 years). As shown in
and where auditory objects are represented in the brain. DeFigure 3, a broad area of activation was seen in the auditory
riving higher-order meaning from the sound we hear is cerareas of the brain. Specifically, activity in response to auditory
tainly a complex process. “Fundamentally, everything that
stimulation was observed both in primary and secondary audicomes into our minds reduces to patterns of neural activity,”
tory cortices. Also of note is that this broad area of auditory
according to Kai-How Farh, MD, a clinical geneticist at Bosactivation occurred bilaterally, even though the participant
ton Children’s Hospital. In other words, each cognitive expewas listening with a CI only on the left ear.
rience is represented by a unique network of neurons that
produces the reality we perceive. For instance, when we
8. Secondary auditory cortex is the launching pad.
hear the word “yellow,” a certain set of neurons responds
Secondary auditory cortex is like the launching pad of the auacross the brain to produce the experience we associate
ditory area of the brain. The complex connections between
with the word. Figure 5a illustrates a network of neurons that
the secondary auditory cortex and the rest of the brain are not
may move across the brain to represent the word “yellow.”
entirely elucidated, but research shows that the secondary
Most of the responsive neurons reside in the primary and
auditory cortex has multiple connections to other areas of the
secondary cortices, but there are also neurons that respond
brain and back to the primary auditory cortex in the form of
from the frontal and parietal lobes (and possibly even in the
efferent tracts. The connections between secondary auditory
cortex and other areas of the brain are often referred to as
Superior longitudinal fasciculus
intra-hemispheric connections. An example is the arcuate fasArcuate fasciculus
ciculus, which connects the temporal and the frontal lobe
(Fig. 4). Numerous others exist, as well as connections to areas inferior to the cerebrum, such as the hippocampus.
The secondary auditory cortex also sends a robust number
of efferent fibers back to primary auditory cortex (i.e., feedback
projections). It has been proposed that efferent fibers from the
Uncinate
fasciculus
secondary auditory cortex likely play a role in tuning the primary
auditory cortex, to focus on primary signals of interest (David.
Inferior longitudinal fasciculus
Proc Natl Acad Sci USA 2012;109:2144). Typical real-world
environments are fraught with a cacophony of speech and environmental noises. For successful communication to occur, the
Figure 4. Illustration of intrahemispheric fiber tracts providauditory system must be able to focus on the acoustic elements
ing connections between different areas within one hemiof the listener’s spoken language—an ability called feature
sphere of the cerebrum (Bhatnagar, 2012).
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a.
b.
sensor motor area
sensor motor area
frontal eye field
frontal eye field
frontal lobe
parietal lobe
prefrontal
area
Broca’s Area
(in left hemsphere)
visual
visual association
temporal lobe
auditory
auditory association
frontal lobe
parietal lobe
prefrontal
area
Broca’s Area
(in left hemsphere)
visual
visual association
temporal lobe
auditory
auditory association
Figure 5. A cartoon representation neural responsiveness (i.e., a neural network or connectome) in response to a. the
word “Yellow,” and b. the sound of bacon frying in a pan. Note, the yellow stars are intended to represent groups of neurons firing in different areas of the brain (Bhatnagar, 2012).
occipital lobe or multimodal areas of secondary auditory cortex).
Engagement of the frontal lobe allows us to extract higherorder meaning from the word “yellow.” For instance, we may
conclude that we dislike the color yellow or that yellow is our
favorite color. Furthermore, we may associate the color yellow
with a traffic light, a canary, a favorite shirt, or a banana. Neurons responding in the frontal and parietal lobes also likely
contribute to our ability to produce or speak the word “yellow.”
Finally, pluripotent neurons in the secondary auditory cortex
or neurons within the occipital lobe interconnected with the
secondary auditory cortex also respond to allow us to form an
image of yellow in our mind’s eye.
Similarly, a unique network or pattern of neurons respond
when we hear bacon frying in a pan (Fig. 5b). That distinct
sizzle in a pan elicits responses from neurons throughout primary and secondary auditory cortices. Even without seeing the
bacon frying in the pan, we can form an image of it in our mind’s
eye because of integration between auditory-responsive neurons in the secondary auditory cortex and visually responsive
neurons. We remember how bacon tastes and feels, and may
even begin to salivate as we hear the frying sound, all because
of the integration between neurons.
In short, each sound that comes into our minds from our ears
is reduced to a unique pattern of neural activity. For that sound
to possess higher-order meaning and come to life, it has to
travel from the primary to the secondary auditory cortex and
form a neural network or connectome with multi-modal areas
throughout the brain. Once again, the secondary auditory cortex
serves as the launching pad for this interaction and integration.
6. Primary auditory cortex was born to hear.
In 1999, Nishimura and colleagues published their groundbreaking research that employed PET scan testing of brain
responses to a variety of stimuli (Nature 1999;397[6715]:116).
The participants were pre-lingually deafened adults who had
no auditory experience and used sign language prior to receiving a CI in adulthood. Nishimura et al. observed neural
activity in the brain in response to three different stimuli: running speech, sign language, and meaningless hand movements. As shown in Figure 6, neural activity was observed in
the primary auditory cortex contralateral to the implanted ear
(but not in the primary auditory cortices of both hemispheres)
when the subjects listened to running speech. This finding
indicates that the primary auditory cortex is hard-wired for
sound. Even when a person does not have access to intelligible speech during the critical
Horizontal sections relative to the intercommissural plane:
period of language develop10 mm below
4 mm above
8 mm above
ment, the primary auditory cortex
still responds to auditory stimuli,
as seen in young adults initially
introduced to sound via CI after a
lifetime of deafness. However, extended duration of deafness likely
reduces the responsiveness and
reorganization of the primary auditory cortex (Kral. Trends Neurosci
2012;35[2]:111). Nonetheless,
the primary auditory cortex remains largely responsive to
sound. This finding may explain
Figure 6. PET scan imaging results showing neural responses in the brain of a pre-­
why adults who never had access
lingually deafened adult with CI after auditory deprivation since birth. Responses are
to sound and communicated via
observed in a. the occipital lobe (in blue) in response to meaningless hand movesign language their entire lives
ments, b. only the secondary auditory cortex (in yellow) in response to a story told
can still detect whisper-level
with sign language, and c. only in the primary auditory cortex contralateral to the imsounds with use of a cochlear implanted ear when a story is spoken while the participant used the cochlear implant for
plant. the left ear (Reproduced with permission: Nishimura. Nature 1999;397[6715]:116).
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