Download Lateralized plastic changes in unilateral hearing loss

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Lateralized plastic changes in unilateral hearing loss
J. T. Devlin1, K. Lanary1, J. Raley1, E. Tunbridge1, A. Floyer-Lea1, C. Narain1, P. Jezzard1, M. Burton2, D. R. Moore3, P. M. Matthews1
1Centre
for Functional Magnetic Resonance Imaging of the Brain, University of Oxford, U. K.
2ENT Department, Radcliffe Infirmary, Oxford, U. K.
3MRC Institute of Hearing Research, Nottingham, U. K.
Results
Summary
Unilateral deafness by cochlear ablation in animals
produces a dramatic increase in the level of neural
activity in the inferior colliculus and auditory cortex
on the side of the intact ear to acoustic stimulation of
that ear. Previous fMRI studies1 appear to confirm this
finding in humans who have unilateral sensorineural
hearing loss. Here we asked whether long term
unilateral hearing loss in humans changes the
symmetry of pure tone BOLD activation in the
supratemporal plane. In primary auditory cortex there
was a clear laterality effect. Relative to silence, tones
presented to the left ear led to greater left hemisphere
activity, as seen previously in normals2. Right ear
stimulation, on the other hand, led to more bilateral
activation – a reduction of the normal left hemisphere
advantage – and this was due to an increase in
ipsilateral activation. In non-primary auditory cortex
unilateral hearing loss did not change the normal
contralateral dominance.
Table 2.
 Monaural tones relative to silence activated Heschl’s
gyrus and adjacent non-primary areas bilaterally
Figure 2: Auditory cortex activations
Right hemisphere
Left hemisphere
PreCS
IPS
CS
SMG
PreCS
PreCS IFS
PT
STG HG Insula
PP
CS
IPS
SMG
PTr
PTr
STS
MTG
TP
 7 sensorineural hearing loss (SNHL)
 5 conductive hearing loss (CHL)
Patients
Significance
0.7% (0.10)
0.5% (0.09)
0.8% (0.08)
0.5% (0.09)
n.s.
n.s.
Right ear stimulation
L. PAC
0.9% (13.4)
R. PAC
0.3% (0.10)
0.9% (0.20)
0.6% (0.12)
n.s.
p<0.08
Left ear stimulation
L. PAC
R. PAC
PT
Insula PP HG STG
MTG
TP
Left ear stimulation
 Thus the reduction in laterality in patients with unilateral
hearing loss in their left ear was due to an increase in
activation in PAC ipsilateral to the stimulated (i.e. right) ear.
Non-primary auditory cortex
 Defined as areas adjacent to PAC which were activated by the
tone vs. silence comparison in the group
Right ear stimulation
HG
removed
Masked
p<10-7
The upper panels display lateral views of the inflated left and right
hemisphere surfaces with sulci and gyri shown in dark and light grey,
respectively. The middle and bottom panels show activation in cortical
auditory fields due to left and right ear stimulation.
 11 patients with long term unilateral hearing loss
Controls
STS
p<0.01
Participants
Mean (±SEM) percent BOLD signal change for
tones relative to silent trials in PAC.
1
2
3
Step 1: Tones vs. silence in RFX (cluster stats: Z>2.3, p<0.05)
Step 2: Anatomically masked to include coordinates of human
non-primary areas4
Step 3: Removed individual subject’s HG
Figure 4: Laterality indices in non-primary areas
 12 normal hearing controls
Left ear stimulation
Laterality calculations
Type of
Affected Duration
Hearing loss Gender Ear
(yrs)
SNHL
F
R
23
SNHL
M
L
20
SNHL
F
R
16
SNHL
M
R
12
SNHL
M
R
12
SNHL
F
L
9
SNHL
M
L
8
CHL
F
L
2
CHL
M
R
6
CHL
F
L
20
CHL
M
R
18
Severity
(threshold) Etiology
Mod.-Sev.
(65-75dB)
Profound
(>90dB)
Profound
(>95dB)
Profound
(>95dB)
Profound
(>95dB)
Profound
(>95dB)
Profound
(>95dB)
Mild
(36.25dB)
Mild-Mod.
(46.25dB)
Moderate
(57.5dB)
Moderate
(60dB)
 To assess relative laterality of auditory cortex
responses, we computed a Laterality Index (LI):
Possibly mumps
Possibly mumps
(Contralateral - Ipsilateral BOLD signal change)
× 100
LI =
(Contralateral + Ispilateral BOLD signal change)
Possibly mumps
+100 indicates completely contralateral activation
-100 indicates completely ipsilateral activation
Unknown
Unknown
 Using mean signal change avoided biasing the
laterality calculation through
(1) an arbitrary statistical threshold for counting
“active” voxels, or
(2) differences in the volume of the ROIs across
hemispheres (i.e. partial volume effects).
Possibly maternal
rubella
Possibly viral
Otosclerosis
Perforated ear
drum
Otosclerosis
Current Study
E.g.:
 The current study used sparse sampling3 to measure
cortical auditory responses to monaurally presented
tones
Figure 3: Laterality indices in PAC
Left ear stimulation
Figure 1: Sparse sampling paradigm
Laterality index
0.5
50
0
5
Tone
10
15
20
25
Time (seconds)
Scanner
Scanner
Tone
30
35
 Participants discriminated between high (4000Hz) and
low (250Hz) frequency tones (90db SPL) by pressing
one of two buttons as quickly as possible after the tone
onset.
 Half of all trials had a silent stimulus.
 The purpose of the task was simply to control attention
by forcing participants to attend to the tones throughout
the scanning.
Normal group means
Right ear stimulation
0.5
50
0.3
30
0.3
30
10
0.1
10
0.1
*
R
-10
-0.1
-10
-0.1
-30
-0.3
-30
-0.3
-50
-0.5
Stimulation
Paradigm
Normal group means
0.1
10
100.1
0.0
0
0.0
0
(p<0.05)
*
(n.s.)
-10
-0.1
-10
-0.1
-20
-0.2
-30
-0.2
 In non-primary auditory cortex, there were no significant
differences between the HL patients and the normal
controls.
Discussion
Like previous studies, we observed a reduction in the
normal contralateral advantage for auditory processing in
patients with unilateral hearing loss1,5. The current study,
however, qualifies these findings in two important ways:
Primary auditory cortex
 The majority of primary auditory cortex (PAC) is located on
Heschl’s gyrus and was therefore identified on each
participant’s structural scan as an anatomic correlate of PAC.
Expected
BOLD signal
200.2
1. Plastic changes were limited to primary auditory cortex and
not found in the adjacent non-primary regions, and
Congenital atresia
of external canal
The threshold value represents the patient’s average for 500Hz, 1kHz,
2kHz, and 4kHz pure tone audiometry.
0.2
20
Laterality index
Table 1. Patient details
Right ear stimulation
n.s.
-50
-0.5
CHL patients
SNHL patients
Patient mean (±SEM)
 For right ear stimulation, HL patients showed a
significant reduction in the normal contralateral
dominance. In fact, there was no significant laterality
effect in these patients.
 There were no significant differences between the HL
patients and the normal controls for left ear stimulation.
Both groups showed a strong ipsilateral (i.e. left
hemisphere) dominance.
2. Only right ear stimulation led to a reduced laterality effect
and this was due to an increase in ipsilateral activation rather
than a reduction in contralateral activity.
If BOLD signal primarily reflects synaptic metabolic
demands6, then the observed changes are consistent with
animal studies showing substantial sub-cortical activation
increases on the side of the stimulated ear. Unlike other
species, however, in humans this effect is only present for
right ear stimulation. This may be due to the fact that humans
appear to be unique in that they display a left hemisphere
dominance for processing simple monaurally presented
auditory stimuli2. In other words, a strong sub-cortical path
already exists in humans leading from the left ear to left PAC
which may not need to be strengthened in the event of hearing
loss in the right ear.
References
1. Bilecen, D., Seifritz, E., Radu, E. W., Schmid, N., Wetzel, S., Probst, R.,
& Scheffler, K. (2000). Cortical reorganization after acute unilateral
hearing loss traced by fMRI. Neurology, 54(3), 765-767.
2. Devlin, J. T., Raley, J., Tunbridge, E., Lanary, K., Floyer-Lea, A., Narain,
C., Cohen, I., Behrens, T. E. J., Jezzard, P., Matthews, P. M., & Moore,
D. R. (in submission). Functional asymmetry for auditory processing
in human primary auditory cortex. (See also Poster #1448.)
3. Hall, D. A., Haggard, M. P., Akeroyd, M. A., Palmer, A. R.,
Summerfield, A. Q., Elliot, M. R., Gurney, E. M., & Bowtell, R. W.
(1999). "Sparse" temporal sampling in auditory fMRI. Human Brain
Mapping, 7, 213-223.
4. Rivier, F., & Clarke, S. (1997). Cytochrome oxidase,
acetylcholinesterase, and NADPH-diaphorase staining in human
supratemporal and insular cortex: Evidence for multiple auditory areas.
NeuroImage, 6, 288-304.
5. Scheffler, K., Bilecen, D., Schmid, N., Tschopp, K., & Seelig, J. (1998).
Auditory cortical responses in hearing subjects and unliateral deaf
patients as detected by functional magnetic resonance imaging.
Cerebral Cortex, 8, 156-163.
6. Logothetis, N. K., Pauls, J., Augath, M., Trinath, T., & Oeltermann, A.
(2001). Neurophysiological investigation of the basis of the fMRI
signal. Nature, 412(6843), 150-157.