#1561
J. T. Devlin 1 , K. Lanary 1 , J. Raley 1 , E. Tunbridge 1 , A. Floyer-Lea 1 , C. Narain 1 , P. Jezzard 1 , M. Burton 2 , D. R. Moore 3 , P. M. Matthews 1
1
2
3
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 studies 1 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 normals 2 . 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.
 Monaural tones relative to silence activated Heschl’s gyrus and adjacent non-primary areas bilaterally
PreCS
IPS
SMG
CS
PreCS IFS
PTr
STG
PT
HG Insula
PP
PTr
STS
MTG
TP
PreCS
CS
IPS
Insula
SMG
PP
HG
PT
STG
STS
MTG
TP
Patients Significance Controls
L. PAC
R. PAC
0.7% (0.10)
0.5% (0.09)
L. PAC
R. PAC
0.9% (13.4)
0.3% (0.10)
0.8% (0.08)
0.5% (0.09)
0.9% (0.20)
0.6% (0.12) n.s.
n.s.
n.s.
p<0.08

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.

Defined as areas adjacent to PAC which were activated by the tone vs. silence comparison in the group
Masked
HG removed p<0.01 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.
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 areas 4
Step 3: Removed individual subject’s HG
(p<0.05)
*

11 patients with long term unilateral hearing loss

SNHL

CHL

12 normal hearing controls
Type of Affected Duration Severity
Hearing loss Gender Ear (yrs) (threshold) Etiology
SNHL
SNHL
SNHL
SNHL
SNHL
SNHL
SNHL
CHL
CHL
CHL
CHL
F
M
F
M
M
F
M
F
M
F
M
R
L
R
R
R
L
L
L
R
L
R
23
20
16
12
12
9
8
2
6
20
18
Mod.-Sev. Possibly mumps
(65-75dB)
Profound Possibly mumps
(>90dB)
Profound Possibly mumps
(>95dB)
Profound Unknown
(>95dB)
Profound Unknown
(>95dB)
Profound Possibly maternal
(>95dB) rubella
Profound Possibly viral
(>95dB)
Mild Otosclerosis
(36.25dB)
Mild-Mod. Perforated ear
(46.25dB) drum
Moderate Otosclerosis
(57.5dB)
Moderate Congenital atresia
(60dB) of external canal
The threshold value represents the patient’s average for 500Hz, 1kHz,
2kHz, and 4kHz pure tone audiometry.

The current study used sparse sampling 3 to measure cortical auditory responses to monaurally presented tones
Tone Tone
0 5 10 15 20 25 30 35
Time (seconds)

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.

To assess relative laterality of auditory cortex responses, we computed a Laterality Index (LI):
LI =
(Contralateral - Ipsilateral BOLD signal change)
× 100
(Contralateral + Ispilateral BOLD signal change)
+100 indicates completely
activation
-100 indicates completely
activation

Using
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).

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.
E.g.:
*
R
±

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.
(n.s.)

In non-primary auditory cortex, there were no significant differences between the HL patients and the normal controls.
Like previous studies, we observed a reduction in the normal contralateral advantage for auditory processing in patients with unilateral hearing loss 1,5 . The current study, however, qualifies these findings in two important ways:
1. Plastic changes were limited to primary auditory cortex and not found in the adjacent non-primary regions, and
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 demands 6 , 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
for processing simple monaurally presented auditory stimuli 2 . 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.
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.
(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.
, 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.
, 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.
, 156-163.
6. Logothetis, N. K., Pauls, J., Augath, M., Trinath, T., & Oeltermann, A.
(2001). Neurophysiological investigation of the basis of the fMRI signal.
(6843), 150-157.