Reversal of Hemispheric Asymmetry on Auditory Tasks in Children

J Am Acad Audiol 13 : 59-71 (2002)
Reversal of Hemispheric Asymmetry
on Auditory Tasks in Children
Who Are Poor Listeners
Rebecca I. Estes*
James Jerger*
Gary Jacobson'
Abstract
We examined hemispheric activation patterns during auditory and visual processing in two groups
of children : 13 boys in the age range from 9 to 12 years rated by their parents and teachers as
poor listeners and 11 boys in the same age range rated as normal listeners. Three tasks were
employed : auditory gap detection, detection of auditory movement, and a control task involving
visuospatial discrimination . Electrical activity was recorded from 30 scalp electrodes as participants responded to target stimuli in an event-related potential paradigm . In the visual task,
hemispheric activation was relatively symmetric around the midsagittal plane in both groups . In
the two auditory tasks, however, hemispheric activation patterns differed significantly between
groups . In the normal-listener group, activation was asymmetric to the right hemisphere . In the
poor-listener group, however, activation tended toward asymmetry, favoring the left hemisphere .
These results suggest that abnormalities in hemispheric lateralization of function may underlie the
auditory processing problems of at least some children described as poor listeners .
Key Words : Auditory processing, children, event-related potential, gap detection, hemispheric
asymmetry, sound movement
Abbreviations : ANOVA = analysis of variance ; APD = auditory processing disorder ; CHAPS =
Children's Auditory Performance Scale ; CT = computed tomography ; CV = consonant vowel ; EEG
= electroencephalographic ; ERP = event-related potential ; fMRI = functional magnetic resonance
imaging ; LPC = late positive component ; SPECT = single-photon emission computed tomography
Sumario
Examinamos patrones de activaci6n hemisferica durante etapas de procesamiento auditivo y
visual en dos grupos de ninos :13 muchachos en el rango de edad de 9 a 12 anos calificados por
sus padres y maestros como portadores de una pobre habilidad para escuchar y 11 muchachos
de el mismo rango de edad calificados con una normal habilidad para escuchar . Tres tareas fueron
utilizadas : detecci6n de brechas auditivas, detecci6n de movimiento auditivo y una tarea de control involucrando discriminaci6n visuoespacial . La actividad electrica fue registrada con 30 electrodos
craneales conforme los participantes respondian a estimulos blanco en un paradigma de potenciales relacionados con el evento (event-related potentials) . En la tarea visual, la activaci6n
hemisferica fue relativamente simetrica en el piano sagital medio en ambos grupos . En las dos
tareas auditivas, sin embargo, los patrones de activaci6n difirieron sign if icativamente entre los
grupos . En el grupo de escucha normal, la activaci6n fue asimetrica al hemisferio derecho. En el
grupo de actitud auditiva pobre, sin embargo, la activaci6n tendi6 hacia la asimetria, favoreciendo
el hemisferio izquierdo . Estos resultados sugieren que pueden haber anormalidades en la lateralizaci6n hemisferica de la funci6n, clue se relacionen con los problemas de procesamiento
auditivo de al menos algunos ninos descritos como portadores de una habilidad pobre para
escuchar.
Palabras Clave : Procesamiento auditivo ; potencial relacionado con el evento ; detecci6n de brecha ;
asimetria hemisferica ; movimiento de sonido
Abreviaturas : ANOVA = analisis de variancia ; APD = trastorno de procesamiento auditivo ; CHAPS
= Escala de Rendimiento Auditivo en Ninos ; CT = tomografia computarizada ; CV = consonantevocal ; EEG = electroencefalografia ; ERP = potencial relacionado con el evento ; IMRI = imagenes
por resonancia magnetica funcional ; LPC = componente positivo tardio ; SPECT = tomografia computarizada por emisi6n de prot6n unico
*Program in Cognition and Neuroscience and The Callier Center for Communication Sciences and Disorders, The
University of Texas at Dallas ; tDivision of Audiology, Henry Ford Hospital, Detroit, Michigan
Reprint requests : James Jerger, 2612 Prairie Creek Dr. East, Richardson, TX 75080-2679
59
Journal of the American Academy of Audiology/ Volume 13, Number 2, February 2002
n spite of normal peripheral hearing sensitivity, some children are characterized by
teachers and parents as poor listeners. They
are described as having difficulty hearing in background noise and in following oral instructions
(Bellis,1996). They are often initially identified by
poor academic performance. In its pure form, the
deficit is conceptualized as an auditory perceptual disorder. In the literature, it is often referred
to as a central auditory processing disorder or,
more appropriately, simply as an auditory processing disorder (APD). Some have suggested that
APD is a factor contributing to dyslexia (Bryden,
1982), specific language impairment (Sloan,1985),
and learning disability (Keith, 1984).
The basis for such an auditory perceptual
problem remains unclear. In the case of language impairment, it has been theorized that the
ability to process rapid temporal changes in
sound is impoverished in some children, resulting in decreased comprehension of spoken communication in settings where multiple inputs and
background competition may be present
(Williams and Lecluyse, 1990 ; Merzenich et al,
1993 ; Tallal et al, 1998). Another factor underlying listening difficulties in children may relate
to deviant cerebral organization. In most normal
children, processing is lateralized to the left
hemisphere for linguistic stimuli and to the
right hemisphere for nonlinguistic stimuli. Thus,
a lack of appropriate lateralization may underlie disordered function . Early studies of hemispheric lateralization relied heavily on behavioral
dichotic tests, usually employing consonantvowel (CV) syllables or CVC words. More
recently, evoked electrical or magnetic potentials,
usually event-related potentials (ERPs), and
brain imaging, usually computed tomography
(CT), functional magnetic resonance imaging
(fMRI), and single-photon emission tomography (SPELT), have addressed the issue as well .
In children with learning disability, abnormal
lateralization of function has been repeatedly
observed on dichotic tests (Keith, 1984 ; Obrzut et
al, 1985 ; Boliek et al, 1988). More recently, Boliek
and Obrzut (1998) compared right-hemisphere
(pure tones) and left-hemisphere (CV syllables)
tasks in both normal and learning-disabled children . Control children had the expected hemispheric laterality shift (to the right for tones and
to the left for CV syllables). In the learning disabled group, however, there was a processing
bias to the same hemisphere (right for some, left
for others) for both types of tasks.
Reversals and other abnormalities of hemispheric specialization have been most exten60
sively studied in children with dyslexia . Bryden
(1982) reviewed a number of studies of lateralization of brain function in children who were
poor readers. In his summary, he remarked that
"Despite unreliable measuring instruments, a
plethora of experimental effects that contaminate
the results, various methodological absurdities,
and frequent instances of contradictory evidence,
one theme continues to recur. That is the notion
that bilateral representation of function [i .e .,
lack of appropriate lateralization] is associated
with deficit" (p . 256-257). Obrzut and colleagues
(1989) employed CV syllables in a dichotic listening framework (free recall, directed right,
directed left) to study cerebral lateralization in
reading-disabled children . Right-handed normal
children showed the expected right-ear advantage
in all three conditions, but right-handed readingdisabled children showed a left-ear advantage in
the free-recall and directed-left conditions In a
dichotic listening study, Hugdahl and colleagues
(1995) compared dyslexics with normal controls
on dichotically presented CV syllables. Controls
showed the expected right-ear advantage, but
dyslexics did not. Similar findings were reported
by Landwehrmeyer and colleagues (1990) . In
the performance of language tasks, normal readers showed greater activation over the left hemisphere, but dyslexics showed greater activation
over the right hemisphere . In a review of CT/MRI
studies of dyslexics, Hynd and Semrud-Clikeman (1989) concluded that the asymmetry toward
the left planum temporale in normal brains was
less often observed in dyslexics. The prevalence
of symmetry (i.e ., lack of appropriate asymmetry) in this key structure for language processing was greater in dyslexics. Similar conclusions
were reached by Hynd and colleagues (1990)
and by Morgan and Hynd (1998) . In a recent
fMRI study of children with developmental
dyslexia, Temple and colleagues (2001) found
that, during letter rhyming, both normal and
dyslexic children showed activity in the left
frontal brain region, but only normals showed
activity in the left temporoparietal cortex .
Dyslexic children failed to show activity in this
cortical region . On a letter-matching task, normals showed activity throughout the extrastriate cortex, but dyslexic children showed little
activity in this region . Using magnetoencephalography, Heim and colleagues (2000)
reported similar differences in the organization
of the left auditory cortex between normals and
dyslexics.
In children with language disorder, a series
of ERP studies have demonstrated reversed
Reversal of Hemispheric Asymmetry in Poor Listeners/Estes et al
hemispheric asymmetry. Dawson and colleagues (1989) compared hemispheric activation
patterns to a simple speech stimulus in both
autistic children and children with severe language impairment . In both groups, there was
a reversed direction of asymmetry relative to
normal children . Similar ERP results for children with specific language impairment were
reported by Shafer and colleagues (2001) . Chiron and colleagues (1999) used the SPECT
technique to measure regional cerebral blood
flow in children with developmental dysphasia .
They concluded that functional specialization
of both hemispheres was impaired in these
children .
Interestingly, similar anomalies and reversals of hemispheric organization have been
reported in stutterers (Salmelin et al, 1998),
schizophrenics (Luchins et al, 1982 ; Holinger et
al, 1992 ; Petty et al, 1995 ; Tiihonen et al, 1998),
the families of schizophrenics (Honer et al, 1995),
deaf persons (Szelag, 1996), and suicidal persons
(Weinberg, 2000).
In a theoretical discussion of these converging lines of evidence for reversal of hemispheric lateralization of function in children
with dyslexia, Stein (1994) suggested that a
specific magnocellular cell type expresses a distinctive surface antigen that plays an important
role in the sequencing of small visual symbols .
Stein suggested that the development of this
cell line may be congenitally impaired in dyslexic
children . He further speculated that normal
magnocellular development promotes normal
hemispheric specialization and that impaired
magnocellular development may be responsible for a spectrum of problems associated with
impaired hemispheric specialization, ranging
from the mildest, dyslexia, to the most severe,
schizophrenia .
Is it possible that the problems faced by
poor listeners may be related to differences in
the functional lateralization of auditory processing? Could the phenomenon of poor listening in children derive from lack of appropriate
lateralization of brain function? The purpose of
the present study was to compare patterns of
hemispheric activation during auditory processing in two groups of children, poor listeners
and normal controls . We employed two auditory processing tasks, gap detection and detection of sound movement, as well as a visual
discrimination control condition. Hemispheric
patterns of activation were evaluated in the
context of scalp electrical activity evoked within
an ERP paradigm .
METHOD
Participants
Participants were recruited from the general
population in the Dallas-Fort Worth metroplex .
Twenty-four children were tested in the Topographic Brain Mapping Laboratory at the University of Texas at Dallas . Informed consent
was obtained from all participants in accordance with the university's guidelines . All children were right-handed males between the ages
of 9 and 12 years . Right-handedness was determined by standard questionnaire and classification (Annett, 1970) . The children had no known
visual or neurologic deficit . All participants had
age-appropriate academic performance as determined by standardized tests of achievement
(23) or teacher report (1) . All participants had
20/25 visual acuity, corrected, using both eyes,
on the Snellen static visual acuity test . Hearing
sensitivity was screened at 20 dB HL at octave
intervals across the frequency range from 250
to 8000 Hz . The experimental participants (n =
13) were identified by both parent and teacher
as "poor listeners" as determined by an at-risk
score on the Children's Auditory Performance
Scale (CHAPS ; Smoski et al, 1998) . No control
child was scored as at risk on the CHAPS by
either the parent or the teacher. Children were
paid for their participation in the study.
EEG Recording System
Electroencephalographic (EEG) activity was
recorded from 30 scalp locations, using silver/silver-chloride (Ag/AgCl) electrodes attached
to an elastic cap (Neurosoft) . The electrode montage placement is based on the International 1020 system . Eye movements and eye blinks were
monitored via electrodes positioned above and
at the outer canthus of the left eye . All channels
of EEG were referenced to linked mastoid electrodes with forehead as ground . Electrode configuration is displayed in Figure 1 . Individual
sweeps of EEG activity, time-locked to the stimuli, were stored for offline analysis . The stored
epoch encompassed -200 to +1400 msec relative
to the onset of each stimulus . The ongoing EEG
activity was sampled at 1000 Hz, amplified,
analog filtered from 0 .15 to 70 Hz (1 .0-100 Hz
for the eye channel), and then digitized through
the Neuroscan acquisition interface system .
Epochs were separately averaged for target and
nontarget stimuli . Signal averaging was conducted after offline artifact rejection and base-
61
Journal of the American Academy of Audiology/Volume 13, Number 2, February 2002
Nose
Left Side
F7
FT7
FPI
F3
Right Side
I
FP2
AFZ
FZ
I
FCZ
FC3
F8
F4
FC4
FT8
--T7 -------- C3 --------- CZ -------- C4 -------- T8 -TP7
CPZ
CP3
P7
P3
01
CP4
PZ
P4
OZ
02
TP8
P8
Figure 1 Electrode array used to record event-related
potential responses to auditory and visual stimuli .
line corrections (Scan 4.1 software). Individual
epochs were examined and rejected whenever
electrical activity in the eye channel exceeded
±50 p,V Each individual ERP was based on a
minimum of 20 acceptable sweeps . In all cases,
this was sufficient to reveal the endogenous
component of the evoked response . Successfully
averaged evoked potential waveforms were then
digitally low-pass filtered at 20 Hz . Filter slope
was -48 dB per octave . Final individual and
grand-averaged waveforms were baseline corrected relative to the 200-msec prestimulus
activity. Topographic maps of the digitally filtered
visual and auditory ERPs were constructed by
interpolation of voltages between adjacent electrodes, using a four-point linear interpolation
algorithm. A bivalent color scheme, representing the range of observed voltages, was assigned
to the resulting voltage matrix .
Rationale for Selection of
Auditory and Visual Tasks
Traditional tests of auditory processing are
plagued by a number of potential confounds.
First, they usually employ linguistic stimuli,
ranging from simple CVs to entire sentences as
test items . But if APD and specific language
impairment can coexist, then linguistic stimuli
may not be the optimal choice for evaluating an
auditory perceptual disorder (Jerger and Allen,
1998). Second, motivational and attentional factors are not always well controlled . Variations in
this dimension may affect absolute performance
62
on difficult tests of speech recognition (cf., Silman
et al, 2000). Third, modality specificity is usually
not demonstrated (McFarland and Cacace, 1995).
Poor test performance may simply reflect, for
whatever reason, poor overall performance on all
modalities . If only the auditory modality is tested,
such dysfunction may be inappropriately attributed to an auditory disorder.
In an attempt to avoid these pitfalls, we
purposely avoided the use of any linguistic test
materials. We chose two auditory tasks, gap
detection and sound movement detection, thought
to be relevant to auditory processing yet executable without the use of linguistic stimuli. Gap
detection is a measure of temporal resolution, an
auditory dimension that has enjoyed considerable
research attention as a result of its putative link
to specific language impairment (Tallal et al,
1998) . We constructed two gap detection tasks.
In one, the gap duration was 30 msec, a value chosen for its location at the "rapid" end of the range
of formant transitions in speech (approximately
20-100 msec ; Kuhl, 1994). In the second gap
detection task, the gap duration was 100 msec,
a value chosen as representative of a comparatively slow formant transition speed.
The second auditory task, detection of sound
movement, was chosen for its relevance to the
question of whether impairment in auditory
spatial perception underlies the problems that
poor listeners have in attending to target speech
in the presence of background competition. We
reasoned that such a spatial disorder might
become manifest as an asymmetry in responses
to sound movement to the right and to the left
of midline.
We addressed the issue of attentional and
motivational factors by structuring the testing
such that cooperation and successful completion of the testing resulted in a modest financial
reward for the child.
We addressed the issue of modality specificity by including a visual control condition.
We reasoned that group differences on both the
auditory and visual tasks would argue against
a modality-specific auditory perceptual disorder.
On the other hand, if performance on the visual
task did not differentiate the two groups, but performance on the auditory tasks did differentiate
them, this would be a strong argument for modality specificity.
Because of fundamental differences in the
auditory and visual systems, it is difficult to
construct true visual analogs of auditory tasks.
For our purposes, we elected to employ a simple visuospatial task, which would at least allow
Reversal of Hemispheric Asymmetry in Poor Listeners/Estes et al
No Gap
us to compare the two groups on a visual task
within the same genre as the auditory tasks .
Right
Auditory Stimuli
Bursts of broadband random noise were created digitally at a sampling rate of 22,050 Hz
with 16-bit amplitude resolution . Stimulus presentation level for noise bursts was 50 dB SPL,
as read on the C scale of a sound level meter, positioned at the location of the center of the par-
Left
30-msec Gap
ticipant's head during testing . Auditory stimuli
were presented through phase-matched loudspeakers positioned at ear height and 1 .5 meters
to either side of participant's ears (Fig . 2) .
Right
Left
Gap Detection Task
The first auditory procedure was a gap detection task in an oddball paradigm . The stimulus
was a noise burst, 500 msec in duration, with a
5-msec rise-decay time . It was presented simultaneously from both the right and left loudspeakers . The listener heard a single noise burst
centered above the head . There were two target
conditions . In one, a silent gap of 30 msec was
inserted in the center of the noise burst. In the
other, a silent gap of 100 msec was inserted in
the center of the burst, revealed by a gap in this
duration region . In the nontarget condition, there
was no gap in the noise burst. Overall duration
was constant at 500 msec in all conditions . Each
target condition (30 or 100 msec) was presented
on 25 percent of trials and the nontarget condition on 50 percent of trials . The total number of
trials was 200. Figure 3 illustrates the waveforms
of the stimuli for the nontarget, 30-msec gap
target, and 100-msec gap target conditions .
Computer Monitor
Right Loudspeaker
Left Loudspeaker
1 meter
1 meter
Figure 2 Arrangement of loudspeakers and computer
screen in the listening chamber. Participant's chair is
adjusted vertically until ear canals are vertically level with
centers of loudspeakers .
100-msec Gap
Right
-o
E
Q
Left
100
200
300
Milliseconds
400
Figure 3 Waveforms of stimuli used in the gap detection tasks . Signal is broadband noise. Overall duration
is constant at 500 msec .
Sound Movement Task
The second auditory task assessed the detection of auditory movement in an oddball paradigm . The target stimulus was a 500-msec burst
of random noise . In the two target conditions, the
noise began in the median plane and appeared
to move overhead, either to the right or to the
left, over a distance of approximately 80 degrees .
In the nontarget condition, the noise burst did
not appear to move but remained in its initial
position in the median plane . To create the two
target conditions, amplitudes were adjusted in
a two-channel editing program . Voltages were
ramped over time in such a way that amplitude
was equivalent in the two channels at burst
onset and then tapered linearly in decreasing
fashion on one channel and increasing linearly
on the other channel . At offset, the level difference was 18 dB . When this two-channel stimulus was played through the two loudspeakers,
63
Journal of the American Academy of Audiology/Volume 13, Number 2, February 2002
Nontarget
No Movement
Right
Left
b
Right
d
Left
100
300
200
Milliseconds
Figure 5 Stimuli used in the visual discrimination
task . Nontarget is a complete octagon. Target is one of
four octagons with a missing line segment.
400
Right
Left
Figure 4 Waveforms of stimuli used in the sound movement task . For the two movement conditions, amplitudes are equivalent at onset but differ by 18 dB at offset .
the listener perceived a noise burst that appeared
to move overhead from midline toward either the
right or the left loudspeaker depending on how
the two channels were ramped . Figure 4 shows
waveforms of the three signals: the nontarget,
the target appearing to move toward the right,
and the target appearing to move toward the left .
Visual Discrimination Task
In the visual discrimination task, the stimuli were a set of octagons, 7.5 cm wide, medium
gray on a black background, subtending a length
and width of 1.56 degrees of arc, and presented
at the center of the computer monitor. The nontarget was a contiguous octagon. There were
four targets; each lacked one of the diagonal
segments . Figure 5 shows the configuration of
the octagon in the nontarget and the four target conditions .
Procedure
Auditory stimuli were presented through
loudspeakers positioned at ear height and 1.5
64
Targets
meters to either side of the participant's ears (see
Fig. 2) . Instructions were conveyed via a computer screen positioned directly in front of the
participant at a distance of 2.2 meters . Prior to
the actual testing of each participant, the sound
levels from the two loudspeakers were adjusted
to achieve median-plane localization for that
participant . For a complete description of the procedure, see Jerger and colleagues (2000) . Briefly,
a 500-msec burst of white noise was presented
from the right loudspeaker at 50 dB SPL. The
presentation level from the left loudspeaker was
then randomly varied in steps of 2 dB over a 22dB range centered at 50 dB SPL. At each level,
the burst was presented three times. The participant then indicated the position in space of
the perceived sound image. Median-plane localization was defined as the midpoint of the range
between consistently right-sided and consistently left-sided judgments.
Written instructions followed by a practice
session for each experimental task familiarized
participants with the task and the stimuli. The
visual discrimination task was tested first, followed by the gap detection task . The sound
movement task was tested last . We chose this
progression from easiest to most difficult to sustain the child's motivation as long as possible .
Short "stand and stretch" breaks were given
between each task as needed . Total ERP testing
time was approximately 40 minutes. To minimize
eye blink artifacts, participants were instructed
to direct their gaze toward a focus point (during
auditory tasks) or to the computer screen (during visual tasks) . To further reduce eye blinks,
a cotton ball was affixed with tape to the top of
each eyelid, and the participant was told to stay
relaxed and blink as little as possible .
Reversal of Hemispheric Asymmetry in Poor Listeners/Estes et al
A response pad containing two response
buttons was used to record behavioral responses .
The participant was instructed to press one button if a target (gap, movement, or missing segment) was heard or seen and the other button
if a nontarget was heard or seen .
Statistical Analysis
Amplitudes, latencies, and amplitude differences were evaluated by means of mixeddesign analyses of variance (ANOVAs) . There
was one between-subjects factor (normal listeners vs poor listeners) . Depending on the
analysis, within-subjects factors included gap
duration (30 or 100 msec) and direction of movement (to right or to left). Statistical significance
was evaluated at an alpha error level of .05 .
Normal Listeners
r P3
P2
Waveforms at Electrode PZ
Figure 6 shows grand-averaged target and
nontarget waveforms at the PZ electrode for the
normal- and poor-listener groups for all three
tasks. Activity at this electrode site was representative of evoked activity throughout the
region of peak positivity. We may identify three
distinct landmarks, labeled P2, N2, and P3 . The
lack of a well-defined N1-P2 complex in response
to stimulus onset is consistent with the observation of Kraus and colleagues (1993) that, in
children in the 7- to 11-year range, the N1-P2
response characteristic of adults is not
observed.The initial peaks in the auditory tasks
represent activity in the P2 and N2 regions.
They are followed by peaks in the 500- to 700msec region (P3), reflecting the ERPs evoked by
a change in the sound stimuli, either a silent gap
or the perception of movement . The visual dis-
~
L
1
Poor Listeners
P2
n
P3
Visual Discrimination
Normal Listeners
P2
RESULTS
or all participants and in all conditions, perF cent correct performance exceeded 80 percent . Comparison was made between averaged
responses based on all epochs versus averaged
responses based only on epochs corresponding to
correct responses. Since there were no discernible
differences between the two averages in any
case, the data presented below are based on
averages of all epochs .
Electrophysiologic results were analyzed in
two ways : first in terms of ERP waveforms at the
midline parietal (PZ) electrode site and second
in terms of hemispheric asymmetry of activation
patterns .
mwe^gnt
~ -- m~etre iea
Tv6et
- Nontarget
P3
8&
Figure 6
1200
Latency (msec)
P3
400
Poor Listeners
800
12,00
Waveforms at electrode PZ for both groups in
all conditions .
crimination task shows an initial peak that represents activity in the P2 region superimposed
on the larger, broader peak (P3) reflecting the
event-related response to the visual targets.
The positivity we have labeled P3 is often called
the late positive component (LPC).
The waveforms for auditory gap detection
reflected little difference between the two groups.
Both the initial, chiefly exogenous components
(P2 and N2) and the subsequent endogenous
ERPs were similar in the two groups and for both
gap conditions .
The waveforms for auditory movement
detection also failed to distinguish the two
groups . The normal listeners appeared to show
a slightly smaller P2 response to the movementright condition, but the difference was not great .
The ERPs to sound movement, in the latency
range from 400 to 800 msec, appear to be larger
for the movement-left condition in the normallistener group, but, again, the difference was not
substantial .
Finally, the visual discrimination responses
in the P2 and ERP regions showed similar findings in the two groups .
Statistical Analysis of ERP Waveforms at
Electrode PZ
At electrode PZ, we extracted two measures
from the waveforms of individual participants :
65
Reversal of Hemispheric Asymmetry in Poor Listeners/Estes et al
Auditory Gap-100 inset
091
Auditory Gap-30 cosec
®
®
Auditory Movement-Leh
Poor Listeners
Normal Listeners
Audior Movement---Right
visual o-rimieaner,
-20
-15
-10
-5
0
Left Hemisphere Greater
5
10
15
20
Right Hemisphere Greater
Figure 10 Means and standard errors of interhemispheric amplitude difference measures for each of the
three tasks.
ence between groups was slightly greater for
movement to the right than to the left .
Statistical Analysis of ERP Asymmetries
These asymmetry data were subjected to
mixed-design ANOVAs . In the case of auditory
gap detection, there was one between-subjects
factor (group) and one within-subjects factor
(gap duration) . The results showed a significant main effect of group (F = 4.49, df = 1, 22, p
= .046) but no significant effect of gap duration
and no significant interaction between group
and gap duration. In the case of auditory movement detection, there was a significant main
effect of group (F = 4.41, df = 1, 22, p =.048) but
no significance for either direction of movement
or the interaction between group and direction
of movement . In the case of the visual discrimination task, there was no significant difference
between groups (F = 0.05, df = 1, 22, p = .826).
DISCUSSION
he principal difference between the experT imental and the control groups in the pre-
sent study was an apparent reversal in the
asymmetry of hemispheric activation during
the processing of the two auditory tasks . A consistent finding across the auditory responses
was increased activation over the right hemisphere in the control group but over the left
hemisphere in the poor-listener group . This suggests the possibility of a difference in the patterns of hemispheric organization between the
two groups, a finding in agreement with previous observations in children with dyslexia, language disorder, and learning disability.
It is appropriate to ask whether these results
can be explained by factors unrelated to hemispheric lateralization . Did the test presentation
level place the poor listeners at a disadvantage?
Were the tasks too difficult for the poor listeners?
These possibilities are effectively ruled out by the
fact that correct behavioral responses exceeded
80 percent in all subjects and all conditions .
Moreover, both the amplitudes and latencies of
the ERP responses at the midline electrode sites
were equivalent in the two groups . The groups
differed only on the direction of hemispheric
asymmetries of the ERP responses .
The studies of reversal in hemispheric asymmetry in children with learning, language, and
reading disabilities cited earlier usually involved
some form of phonologic processing task . On
such tasks, normal groups showed expected
asymmetry toward the left hemisphere, whereas
non-normal groups showed either lack of such
asymmetry or asymmetry toward the right hemisphere . In the present study, however, we were
careful to avoid tasks involving linguistic stimuli in order to study the processing of simple
auditory signals uncontaminated by language
processing . The two auditory tasks involved
either the detection of a temporal gap in broadband noise or the detection of movement of the
noise . Both tasks showed the expected asymmetry toward the right hemisphere in the normal group but either lack of such asymmetry or
asymmetry toward the left hemisphere in the
poor-listener group .
There are, however, inherent problems with
inferring, from multichannel voltage field recordings, what is taking place deep within the brain .
That is, for any given scalp voltage "map," there
are an infinite number of possible permutations
of brain events that could give rise to the
observed voltage field . These vagaries are associated with the so-called "inverse" solution . They
are magnified in evoked potential recordings
and minimized in evoked magnetic field recordings . Nevertheless, in the present investigation,
we did observe that children described as normal listeners showed statistically different scalp
distributions for the LPC than did children who
were described as poor listeners . Specifically,
for the auditory tasks, only poor listeners showed
a voltage distribution that was greatest over
the left hemisphere, whereas normal listeners
showed a maximum LPC voltage distribution
over the right hemisphere . The LPC is an
endogenous response that is dependent on the
listener recognizing the significance of a given
"rare" or "target" auditory event that is placed
69
Journal of the American Academy of Audiology/Volume 13, Number 2, February 2002
within a stimulus train of "common" or "frequent" or "nontarget" auditory events . From
invasive depth recordings in humans undergoing neurosurgical procedures (e .g., Halgren et al,
1980) and from noninvasive magnetoencephalographic recordings in humans (e .g .,
Okada et al, 1983), it has been found that the
LPC derives its neural origins from the hippocampus, amygdala, and possibly thalamic or
suhthalamic generators (e .g ., Velasco et al, 1986).
There is evidence that this response is modality specific . That is, the scalp distribution of the
LPC differs when the stimuli are presented to
the auditory, as opposed to visual, modality.
Also, the current belief is that the amplitude of
the LPC is related to the allocation of attentional resources, and the latency of the LPC is
related to the speed at which those resources are
allocated (Polich, 1993). In the present paradigm,
the stimuli were presented binaurally, and,
accordingly, it is likely that activation of LPC
generators occurred bilaterally. As such, one
might have expected a bilateral, symmetric voltage distribution (as was seen when visual stimuli were presented), but this was not observed .
There could be several explanations for the
observed asymmetries. During bilateral activation for normal subjects, the right hemisphere
source(s) may predominate (greater amplitude
of the LPC recorded from that hemisphere),
and, hence, the distribution of activity may
slightly favor the right hemisphere . Alternatively, sources may be activated at equal strength
bilaterally, but the timing of the onsets and
peaks of these voltage fields may differ slightly
in such a way that the right hemisphere shows
the greatest magnitude. Finally, the dipole
strengths may be identical, but the orientation
of the dipoles may differ slightly so that the
scalp voltage field appears greater over the right
hemisphere . We were not able to sort this out
using the current techniques . In the future, it
is possible that we might estimate what is occurring beneath the scalp surface using dipole localization techniques designed to deconvolve
multiple coactivated sources. The findings of
the current investigation suggest that the underlying neurophysiologic mechanisms resulting
in the scalp distribution observed for the normal
listeners are not occurring for the poor listeners.
The differences in the asymmetries in the voltage fields for the two groups may have occurred
because of differences in the strengths of the two
groups of generators or differences in the timing and/or orientation of the generator sources.
70
The reversal of asymmetry of brain activation observed in our poor-listener group appears
to be auditory specific . On the visual task, no difference between groups was observed. We cannot, however, exclude the possibility that a
different visual task might show such reversal .
It remains to be determined whether this reversal of asymmetry between normal and poor listeners would be present but reversed in the case
of linguistic processing. In any event, it seems
possible that abnormalities in hemispheric lateralization of function may underlie the auditory
processing problems of at least some children
described as poor listeners . With further refinement in technique, reversal of hemispheric asymmetry might serve as a biologic marker of the
poor-listener syndrome .
Acknowledgment . We are grateful to Robert Keith for
helpful comments on an earlier version of this report .
Supported in part by a grant from the Excellence in
Education Fund of the University of Texas at Dallas
Callier Center for Communication Disorders .
REFERENCES
Annett M. (1970). Aclassification of hand preference by
association analysis . Br J Psychol 61 :303-321 .
Bellis T. (1996) . Assessment and Management of Central
Auditory Processing Disorders in the Educational Setting.
San Diego, CA: Singular.
Boliek C, Obrzut J. (1998) . Perceptual laterality in developmental learning disabilities . In: Davidson R, Hugdahl
K, eds. Brain Asymmetry. Cambridge : MIT Press,
637-658.
Boliek C, Obrzut J, Shaw D. (1988) The effects of hemispatial and asymmetrically focused attention on dichotic
listening with normal and learning-disabled children .
Neuropsychologia 26 :417-433 .
Bryden M. (1982) . Laterality : Functional Asymmetry in
the Intact Brain . Perspectives in Neurolinguistics,
Neuropsychology, and Psycholinguistics. New York :
Academic Press.
Chiron C, Pinton F, Masure M, et al . (1999) . Hemispheric
specialization using SPECT and stimulation tasks in
children with dysphasia and dystrophia . Dev Med Child
Neural 41 :512-520 .
Dawson G, Finley C, Phillips S, Lewy A . (1989). A comparison of hemispheric asymmetries in speech-related
brain potentials of autistic and dysphasic children. Brain
Lang 37 :26-41 .
Halgren E, Squires N, Wilson C, et al . (1980) . Endogenous
potentials generated in the human hippocampal formation and amygdala by infrequent events . Science
210:803-805 .
Heim S, Eulitz C, Kaufmann J, et al . (2000) . Atypical
organisation of the auditory cortex in dyslexia as revealed
by MEG. Neuropsychologia 38 :1749-1759 .
Reversal of Hemispheric Asymmetry in Poor Listeners/Estes et al
Holinger D, Faux S, Shenton M, et al . (1992) . Reversed
temporal region asymmetries of P300 topography in leftand right-handed schizophrenic subjects . EEG Clin
Neurophysiol 84 :532-537 .
Okada YC, Kaufman L, Williamson SJ. (1983) . The hippocampal formation as a source of the slow endogenous
potentials . Electroencephalogr Clin Neurophysiol
55 :417-426 .
Honer G, BassettA, Squires-Wheeler E, et al . (1995) . The
temporal lobes, reversed asymmetry and the genetics of
schizophrenia. Neuroreport 7:221-224 .
Petty RG, Barta PE, Pearlson GD, et al . (1995) . Reversal
of asymmetry of the planum temporale in schizophrenia.
Am J Psychiatry 152 :715-721 .
Hugdahl K, Helland T, Faerevaag MK, et al . (1995) .
Absence of ear advantage on the consonant-vowel dichotic
listening test in adolescent and adult dyslexics: specific
auditory-phonetic dysfunction. J Clin Exp Neuropsychol
17 :833-840 .
Polich J. (1993) . P300 in clinical applications : meaning,
method and measurement. In : Niedermeyer E, Lopes da
Silva F, eds. Electroencephalography: Basic Principles,
Clinical Applications, and Related Fields . Baltimore:
Williams and Wilkins, 1005-1018.
Hynd G, Semrud-Clikeman M. (1989) . Dyslexia and brain
morphology. Psychol Bull 106 :447-482 .
Hynd G, Semrud-Clikeman M, Lorys A, et al . (1990) .
Brain morphology in developmental dyslexia and attention deficit disorder/hyperactivity. Arch Neural
47 :919-926 .
Jerger J, Greenwald R, Wambacq 1, et al . (2000) . Toward
a more ecologically valid measure of speech understanding
in background noise. J Am Acad Audiol 11 :273-282 .
Jerger S, Allen J. (1998) . How global behavioral tests of
central auditory processing may complicate management.
In : Bess F, ed . Children with Hearing Impairment.
Contemporary Rends. Nashville : Bill Wilkerson Center
Press, 163-177.
Keith R. (1984) . Dichotic listening in children . In : Beasley
D, ed . Audition in Childhood: Methods of Study. San
Diego: College-Hill Press, 1-24.
Kraus N, McGee T, Carrell T, et al . (1993) . Speech evoked
cortical potentials in children . J Am Acad Audiol
4:238-248 .
Kuhl P. (1994) . Speech perception . In : Minifie F, ed .
Introduction to Communication Sciences and Disorders .
San Diego, CA : Singular, 77-148 .
Salmelin R, Schnitzler A, Schmitz F, et al . (1998) .
Functional organization of the auditory cortex is different in stutterers and fluent speakers . Neuroreport
9:2225-2229 .
Shafer V, Schwartz R, Mor M, et al . (2001) . Neurophysiological indices of language impairment in children .
Acta Otolaryngol (Stockh) 121:297-300 .
Silman S, Silverman C, Emmer M. (2000) . Central auditory processing disorders and reduced motivation : three
case studies. JAm Acad Audiol 11 :57-63 .
Sloan C. (1985) . Language, language learning, and language disorder : implications for central auditory
processing . In : Katz J, Stecker N, Henderson D, eds.
Central Auditory Processing: A Transdisciplinary View .
St . Louis: Mosby-Yearbook, 179-186.
Smoski W, Brunt M, Tannahill C. (1998) . C.H.A .P.S .
Children's Auditory Performance Scale Instruction
Manual . Tampa, FL : The Educational Audiology
Association.
Stein J. (1994) . Developmental dyslexia, neural timing
and hemispheric lateralisation . Int J Psychophysiol
18 :241-249 .
Landwehrmeyer B, Gerling J, Wallesch C. (1990) . Patterns
of task-related slow brain potentials in dyslexia . Arch
Neurol 47 :791-797 .
Szelag E. (1996) . The effect of auditory experience on
hemispheric asymmetry in a post-lingually deaf child: a
case study. Cortex 32 :647-661 .
Luchins D, Weinberger D, Wyatt R. (1982) . Schizophrenia
and cerebral asymmetry detected by computed tomography. Am J Psychiatry 139 :753-757 .
Tallal P, Merzenich M, Miller S, Jenkins W. (1998) .
Language learning impairment : integrating research and
remediation . Scand J Psychol 39 :197-199 .
McFarland D, Cacace A. (1995) Modality specificity as a
criterion for diagnosing central auditory processing disorders . Am JAudiol 4:36-48 .
Temple E, Poldrack RA, Saladis J, et al. (2001) . Disrupted
neural responses to phonological and orthographic processing in dyslexic children: an fMRl study. Neuroreport
12 :299-307 .
Merzenich M, Schreiner C, Jenkins W Wang X. (1993) .
Neural mechanisms underlying temporal integration,
segmentation and input sequence representation . Ann
NYAcad Sci 682:1-22.
Morgan A, Hynd G. (1998) . Dyslexia, neurolinguistic ability, and anatomical variation of the planum temporale.
Neuropsychol Rev 8:79-83 .
Obrzut J, ObrzutA, Bryden M, Bartels S. (1985). Information
processing and speech lateralization in learning-disabled
children. Brain Lang 25 :87-101.
Obrzut J, Conrad P, Boliek C. (1989) . Verbal and nonverbal auditory processing among left-and right-handed
good readers and reading-disabled children .
Neuropsychologia 27 :1357-1371 .
Tiihonen J, Katila H, Pekkonen E, et al . (1998) . Reversal
of cerebral asymmetry in schizophrenia measured with
magnetoencephalography. Schizophr Res 30 :209-219 .
Velasco M, Velasco F, Velasco AL, et al. (1986). Subcortical
correlates of the P300 potential complex in man to auditory stimuli. EEG Clin Neurophysiol 64 :199-210 .
Weinberg I. (2000) . The prisoners of despair: right hemisphere deficiency and suicide. Neurosci Biobehav Rev
24:799-815 .
Williams M, Lecluyse K. (1990) . Perceptual consequences
of a temporal processing deficit in reading disabled children . JAm Optom Assoc 61 :111-121 .
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