418 Electroencephalography and clinicalNeurophysiology, 86 (1993) 418-427

© 1993 Elsevier Scientific Publishers Ireland, Ltd. 0013-4649/93/$06.00

EEG 92578

Auditory processing in visual brain areas of the early

blind: evidence from event-related potentials *
K. Alho, T. Kujala, P. Paavilainen, H. Summala and R. N i it inen
Department of Psychology, University of Helsinki, SF-O0014 Helsinki (Finland)

(Accepted for publication: 11 January 1993)

Summary Auditory event-related potentials (ERPs) were recorded in early blind subjects and sighted controls when they attended to
stimuli delivered to a designated ear under dichotic conditions. The scalp distribution of the processing negativity (PN), the endogenous
negativity elicited by attended stimuli, was in the blind posterior to that in the sighted. This suggests that posterior brain areas normally involved
in vision participate in auditory selective attention in the early blind. Furthermore, occasional higher-frequency tones in the to-be-ignored ear
elicited a negativity (presumably the mismatch negativity; MMN) that had a posterior scalp distribution in the blind as compared to controls. This
suggests that the posterior brain areas of the blind also participate in processing of auditory stimulus changes occurring outside the focus of
attention.

Key words: Blind; Visual deprivation; Audition; Attention; Event-related potentials

Blindness beginning at an early developmental stage
modifies processing in the non-deprived sensory
modalities. Early binocular deprivation increases the
proportion of neurons responsive to tactile stimuli dur-
ing a somatosensory task in the occipital (Brodmann's
area 19) and parietal (area 7) cortices of the monkey
(Hyv~irinen et al. 1981a,b; Carlson et al. 1987). Consis-
tent with this, Uhl et al. (1991) found that negative DC
potential shifts associated with a tactile task were larger
over the occipital scalp in early blind humans than in
sighted controls.
Early blindness also affects auditory processing. The
blind may develop an ability to use echoes in order to
perceive spatial positions of objects (e.g., Strelow and
Brabyn 1982). Development of such auditory abilities
in the blind might be related to changes in the auditory
system. For example, Ryugo et al. (1975) found that
early visual or somatosensory deafferentation increases
the density of dendritic spines in the auditory cortex of
the rat. Furthermore, Merzenich et al. (1984) suggested
that even in normal development of the auditory sys-
tem, the cortical mechanisms for sound localization are
Correspondence to: Kimmo Alho, Department of Psychology, P.O.
Box 11, University of Helsinki, SF-00014 Helsinki (Finland).
Tel.: (3580) 191 3407; Fax: (3580) 191 3443.
* This research was supported by the University of Helsinki and the
Academy of Finland. The authors wish to thank the anonymous
referees for their constructive comments and criticism.
dynamically maintained and altered throughout life.
This plasticity is necessary because of changes in bin-
aural localization cues which occur as a result of fac-
tors such as the growth of the head and external ears
during development and with hearing loss related to
aging.
Intracranial recording of evoked potentials in the
cat has shown that early auditory deprivation leads to
enhanced responsiveness of primary auditory cortex to
visual stimuli (Rebillard et al. 1977). Furthermore,
Neville et al. (1983) found larger visual event-related
potentials (ERPs) over temporal and frontal scalp ar-
eas in congenitally deaf human adults than in hearing
controls. This suggests that congenital deafness causes
enhanced visual processing in brain areas normally
participating in audition (see also Neville and Lawson
1987).
In early blind humans, the negative N1 deflection
(peak at about 100 msec from stimulus onset) and the
subsequent positive P2 and P3 deflections of auditory
ERPs show shortened latencies and enhanced ampli-
tudes (Niemeyer and Starlinger 1981; Woods et al.
1985). However, there has been no indication that
cortical areas normally involved in vision participate in
auditory processing in the blind. Although Wanet-De-
falque et al. (1988) found higher occipital glucose
metabolism (measured with positron emission tomogra-
phy; PET) in early blind subjects than in blindfolded
controls during auditory and tactile discrimination
tasks, a similar difference was also found in a resting
A U D I T O R Y ERPs IN BLIND
condition. Therefore, the differences in occipital
metabolism observed during the discrimination tasks
between the blind and sighted appear to have been
caused by a general enhancement of occipital glucose
metabolism associated with blindness.
The present purpose was to determine whether scalp
distributions of auditory ERPs suggest participation of
visual cortex in auditory attention in early blind sub-
jects. To this end, the processing negativity (PN), the
principal ERP index of auditory selective attention
(N~i~it~inen 1982, 1990, 1992), was studied in early blind
subjects and in sighted controls. Subjects attended to
tone pips delivered to a designated ear, in order to
detect occasional deviant (higher) tones occurring
among these tones, and ignored tones delivered to the
opposite ear. PN causes a negative displacement of the
ERP to attended stimuli in relation to that elicited by
unattended stimuli. PN consists of at least two consec-
utive, partially overlapping, components. The earlier
PN component commences at the time zone of the N1
deflection and reaches its maximum amplitude at
fronto-central scalp sites. This PN component is gener-
ated in the auditory cortex (see also Hari et al. 1989),
presumably by a neural matching process selecting
attended stimuli for further processing on the basis of
their physical features (N~i~it~inen 1982, 1990, 1992;
Alho et al. 1986b, 1987a,b, 1989). The later PN compo-
nent peaks at around 300-400 msec from stimulus
onset and might be generated by a frontal source
(Giard et al. 1988) presumably associated with control
of attention (N~i~it~inen 1982, 1990, 1992; N~i~it~inen and
Picton 1987).
ERPs to the higher tones infrequently occurring
among attended and unattended tones were also exam-
ined. Such deviant stimuli elicit the mismatch negativ-
ity (MMN; N~i~it~inen et al. 1978; for reviews, see
N~iat~inen 1990, 1992), a change-specific ERP compo-
nent, which overlaps with the N1 and subsequent P2
components. The change-detection process generating
MMN appears to be automatic since MMN is elicited
even by deviant stimuli occurring among unattended
stimuli (N~i~it~inen et al. 1978; Sams et al. 1985; Alho et
al. 1989, 1992; Woods et al. 1992; see, however,
Woldorff et al. 1991, and for a reply, Na~it~inen 1991).
MMN consists of at least two temporally overlapping
components, one generated in the supratemporal audi-
tory cortex (e.g., Hari et al. 1984; Scherg et al. 1989;
Javitt et al. 1991; Paavilainen et al. 1991) and the other
in the frontal cortex (Giard et al. 1990; Na~it~inen and
Michie 1979). While the supratemporal MMN compo-
nent is presumably generated by a neural change-de-
tection process, the process generating the frontal
MMN component might underlie involuntary orienting
of attention towards this change (N~i~it~inen 1990, 1992;
Alho 1992). The fronto-centrally maximal positive P3a
component often following MMN to deviant stimuli of
419
unattended auditory input is probably associated with
such involuntary orienting of attention (e.g., Naat~inen
et al. 1982; N~i~it~inen and Gaillard 1983; Sams et al.
1985). When a deviant stimulus occurs in an attended
input, MMN is partially overlapped by a negative N2b
component and by the early phase of a parietal P3b
component (N~i~it~inen et al. 1982, 1986).
In sum, while PN is generated by brain mechanisms
of selective attention, ERP components elicited by
stimulus change in an unattended auditory input, espe-
cially MMN and P3a, may reflect mechanisms of auto-
matic auditory processing and involuntary attention.
The purpose of the present study was to examine
whether in the early blind these ERP components
differ from those in the sighted. Possible group differ-
ences might result from differential development of
brain mechanisms of auditory processing.
Methods
Subjects
There were 9 blind (aged 20-29 years) and 9 nor-
mally sighted (aged 19-25 years) subjects, 3 males and
6 females in each group. All subjects were students and
participated voluntarily to the experiment. None of
them had previously served as subjects in similar exper-
iments. All blind subjects had a diagnosed peripheral
deficit which caused early blindness beginning within
the first two years of life. Four of them had a retinopa-
thy of prematurity, one had an inherited retinal degen-
eration, one's peripheral blindness was caused by the
mother's rubella during pregnancy, one's eyes had been
ablated because of retinal cancer, and one had suf-
fered congenital atrophy of the optic tracts. For one
subject, the cause of blindness, diagnosed as periph-
eral, was unknown. Five blind subjects reported that
they could still differentiate between dark and light. In
addition, one subject had been capable of doing so up
to the age of 5 years and another up to the age of 2
years. According to their own reports, none had any
contour or pattern vision, and none could discriminate
the direction of light. In addition, seven of the blind
subjects were presented with flash stimuli in another
study (Kujala et al. 1993) and no visual ERPs were
found, while in sighted controls the flashes elicited
sizeable ERPs.
Experimental procedure
The experiment was carried out in an electrically
and acoustically shielded, dimly lit room. Monaural
tone pips (sine-wave bursts, duration 60 msec including
10 msec rise and fall times, intensity 75 dB SPL) were
presented through headphones in random order to the
left and right ears at a constant rate of 1 tone/610
msec in blocks of 500 stimuli. There were two types of
420
tone in each ear: 600 Hz standard tones (probability
for each ear 0.45) and 650 Hz deviant tones (probabil-
ity for each ear 0.05). Subjects were instructed to
attend to the tones presented to the designated ear (2
blocks in each condition) and to count silently the
deviant tones occurring in that ear. The order of the
conditions was counterbalanced within each group.
Subjects were instructed to avoid eye movements and
blinking during the attention tasks.
EEG recording and analysis
The E E G (0.1-100 Hz, - 3 dB points)was recorded
with Ag/AgC1 electrodes at 19 scalp sites. In addition,
two E O G electrodes were attached laterally to the
outer canthi of the left and right eyes in order to
monitor voltage changes caused by horizontal eye
movements. Activity caused by vertical eye movements
or blinks was recorded with a frontopolar E E G elec-
trode (Fpz). All E E G and E O G electrodes were re-
ferred to an electrode attached to the nose.
The E E G analysis epochs of 420 msec (sampling
rate 250 Hz) began 50 msec before each stimulus onset.
The first 10 epochs of each block, as well as epochs
contaminated by blinks, eye movements, muscle activ-
ity, or other extracerebral artifacts (voltage variation
during an epoch exceeding 150 /xV at any electrode)
were automatically rejected from averaging. Frequen-
cies higher than 30 Hz were digitally filtered out (FFT
filter) from the ERPs.
To study PN, attended-unattended difference waves
were formed for each subject by subtracting, separately
for each ear, ERPs to standard tones when they were
unattended from ERPs to the same tones when at-
tended. In addition, to study E R P components elicited
by deviant tones, deviant-standard difference waves
were formed, separately for the attended and unat-
tended tones, by subtracting ERPs to standard tones
from ERPs to deviant tones.
For statistical comparisons, E R P and difference
wave amplitudes were measured for each subject, in
reference to the 50 msec prestimulus baseline, as mean
voltages over consecutive 50 msec periods within 350
msec from stimulus onset. In addition, N1 peak laten-
cies were determined at Cz and N1 amplitudes at each
electrode were measured at these peak latencies.
To compare scalp distributions of E R P and differ-
ence wave amplitudes between the two groups, these
amplitudes were normalized. This was done separately
for each subject and each measurement period by
dividing the amplitude at each electrode by the square
root of the sum of the squared amplitudes at the
electrodes included in the analysis (McCarthy and
Wood 1985).
In the statistical analysis of E R P and performance
data, analyses of variance included in the BMDP Sta-
tistical Software (Dixon et al. 1988) were used. In
K. ALHO ET AL.
Results, the reported significance levels for the F val-
ues are corrected with a Greenhouse-Geisser correc-
tion where appropriate.
Results
Performance
The reported number of deviant target tones dif-
fered from the correct number on average by 10.0%
and 12.6% in the blind and sighted groups, respec-
tively. According to an analysis of variance, the differ-
ence between the two groups was insignificant.
ERPs to standard tones
At the top of Fig. 1, grand-average ERPs to at-
tended and unattended standard tones are superim-
posed separately for the two groups. The N1 deflection
to the unattended standard tones tended to be larger
and somewhat later in the sighted (mean peak ampli-
tude at Cz - 3 . 9 / ~ V ; mean peak latency 94 msec) than
in the blind ( - 2 . 4 / z V , 90 msec), but these differences
were statistically insignificant. Moreover, an analysis of
variance (factors: Group, Ear, Electrode) for normal-
ized (see Methods) unattended-tone N1 amplitudes
(measured at the N1 peak latency determined at Cz)
showed no differences between the two groups in the
N1 midline distribution (electrodes Fpz, Fz, Cz, Pz,
Oz) or in the N1 distribution on a tilted coronal line
crossing the approximate locations of left and right
auditory cortices (electrodes Mc, Tc, FCc, Fz, FCi, Ti,
Mi; see Fig. 1, top).
In both groups, ERPs to attended standard tones
were negatively displaced in relation to those to unat-
tended standard tones. These displacements, presum-
ably caused by PN, are shown by attended-unattended
difference waves at the bottom of Fig. 1. In both
groups, these displacements were largest at fronto-
central scalp sites. Analyses of variance (factors: Group,
Attention, Ear) for the standard-tone E R P amplitudes
at Fz indicated significant effects of attention over
consecutive 50 msec periods between 100 and 350 msec
( F (1, 16) varied between 23.67 and 48.10, P < 0.001 in
all cases).
At Fz no significant differences in the PN amplitude
(measured from attended-unattended difference waves)
between the two groups were found, whereas at the
posterior scalp sites, this amplitude was larger for the
blind than for the sighted (Fig. 1, bottom). In the blind,
prominent PNs were observed even at occipital elec-
trodes (at Oz, mean PN amplitudes measured over the
consecutive 50 msec periods between 100 and 350 msec
varied from - 0.5/zV to - 1.3 tzV), while in the sighted,
the occipital PN amplitudes approximated 0 /zV. A
comparison of PN amplitudes at occipital electrodes
AUDITORY ERPs IN BLIND 421

(TOc, Oc, Oz, Oi, T O i ; see Fig. 1, b o t t o m ) i n d i c a t e d v a r i a n c e (factors: G r o u p , Ear, E l e c t r o d e ) for n o r m a l -

significant differences b e t w e e n the two groups at 2 5 0 - ized P N a m p l i t u d e s at the m i d l i n e (Fpz, Fz, Cz, Pz,
300 msec ( F (1, 1 6 ) = 4.53, P < 0.05) a n d 3 0 0 - 3 5 0 Oz). T h e s e analyses i n d i c a t e d significant G r o u p x
msec F (1, 1 6 ) = 4.83, P < 0.05) a n d n e a r l y significant E l e c t r o d e i n t e r a c t i o n s over all consecutive 50 msec
differences at 1 5 0 - 2 0 0 msec ( F (1, 16) = 3.11, P < 0.10) periods b e t w e e n 100 a n d 350 msec from stimulus o n s e t
a n d 2 0 0 - 2 5 0 msec ( F (1, 16) = 3.89, P < 0.07). ( F (4, 64) varying from 4.20 to 5.66, P < 0.05 in all
Thus, in the blind, P N was d i s t r i b u t e d posteriorly to cases). I n contrast, n o significant G r o u p × Electrode
that in the sighted. This was c o n f i r m e d by analyses of i n t e r a c t i o n s were f o u n d in analogous analyses of vari-

ERPs TO STANDARDS
- - ATTENDED
........ U N A T T E N D E D

.,••_•GHTED
FCi~ _ -~

•..... .... .....". ~

' ..."....~ . .:.,..,......

Mi c~A ~ Mo .......... ,....

"......
~....- ..,

\ / \ /
p• Pz
A
P c ~
.&
" ............
~ .
POi ~ ~.............
' " - " - " P~O c ..............
TO
. ~i Oi~ . - .,.... O z " " '-....- T O c
• .,... ......., • ..... ...

-2pV]~
0 300ms
DIFFERENCE" ATT-UNATT
BLIND
........ SIGHTED

\ /
. .. .. . . . . --.., . . . , ....

. . . . . .~ . . . . . .., . . , ... .....,. .. ....,.

Fig. 1. Top: grand-average ERPs at different scalp sites to attended (solid lines) and unattended (dashed lines) standard tones in the blind (left;
n = 9) and sighted (right; n = 9). The ERPs were averaged across the left and right ear standard tones. Before combining the data for the left and
right ear stimuli, the ERPs to the right ear stimuli over the lateral scalp sites were mirrored to the opposite hemisphere. Thus, the ERPs at scalp
sites contralateral to the stimulated ear are shown over the right hemisphere and the ERPs at scalp sites ipsilateral to the stimulated ear are
shown over the left hemisphere (stimulus onset at 0 msec; c = contralateral; i = ipsilateral; HEOGc and HEOGi electrodes located at the outer
canthi of the eyes, used for monitoring EOG changes caused by horizontal eye movements; Mc and Mi are electrodes at the mastoids; FCc/FCi
and Tc/Ti were equidistantly placed between Fz-Mc or Fz-Mi; Pc/Pi are the sites P3/P4; Oc/Oi are the sites O1/O2; OPc/OPi located
halfway between Oz and P3/P4; TOc/TOi located halfway between O1-T5 or O2-T6). Bottom: difference waves for the blind (solid lines) and
sighted (dashed lines) formed by subtracting the grand-average ERPs to standard tones when unattended from the ERPs to the same tones when
attended.
 422
K. ALHO ET AL.

ance for normalized PN amplitudes.on a tilted coronal
line (electrodes Mc, Tc, FCc, Fz, FCi, Ti, Mi; see Fig.
1, bottom)•
At most scalp sites, the attended-tone ERPs, as well
as the unattended-tone ERPs, were more positive in
the blind than in the sighted (Fig. 1, top). At the
midline electrodes (Fpz, Fz, Cz, Pz, Oz), this group
difference was significant for the attended standard
tones at 100-200 msec (100-150 msec: F (1, 16) = 7.01,
P < 0.02; 150-200 msec: F (1, 16) = 6.17, P < 0•025)
and for the unattended standard tones at 50-200 msec
(50-100 msec: F (], 16) = 7.08, P < 0.02; 100-150 msec:
F (1, 16) --- 7.72, P < 0.015; 150-200 msec: F (1, 16) =
4.75, P < 0.05). No significant Group × Electrode in-
teractions were found in analyses of variance (factors:
Group, Ear, Electrode) for normalized midline ampli-
tudes of the unattended-standard ERPs at consecutive
50 msec periods between 50-350 msec, whereas analo-
gous analyses for attended-standard ERPs indicated a
significant Group × Electrode interaction at 300-350
msec ( F (4, 64)= 3.19, P < 0.02) and a nearly signifi-
cant Group × Electrode interaction at 200-250 msec
(F (4, 64) = 2.23, P < 0.08). These interactions suggest
that the posterior distribution of the attended-un-
attended difference waves in the blind was indeed due
to an effect of blindness on ERPs to attended tones
rather than on ERPs to unattended tones. Thus, these
analyses also support the proposal that the PN elicited

ERPs TO UNATTENDED TONES

........ STANDARD
DEVIANT
BLIND ~.~.~.~, SIGHTED

• • ;:..... ....

:/

\ /

-2pvL_
o 360ms

DIFFERENCE: DEV-STAND
BLIND
........ SIGHTED

A,

\ /

Fig. 2. Top: grand-average ERPs in the blind and sighted to standard (dashed lines) and deviant (solid lines) tones of unattended stimulus
sequence. (For further details, see Fig. 1.) Bottom: difference waves for the blind (solid lines) and sighted (dashed lines) groups formed by
subtracting the grand-average ERPs to standard tones of unattended stimulus sequence from the ERPs to deviant tones of the same sequence.
A U D I T O R Y ERPs IN BLIND 423

by the attended tones was posteriorly distributed in the
blind.
ERPs to deviant tones
For the unattended ear, deviant-tone ERPs were
negatively displaced in relation to standard-tone ERPs
in both groups (Fig. 2, top). This negative displacement
was largest at fronto-central scalp sites, as shown by
the deviant-standard difference waves at the bottom of
Fig. 2. Analyses of variance (factors: Group, Ear, Stim-
ulus) for unattended-ear ERP amplitudes at Fz indi-
cated that this negative displacement was significant at
100-250 msec (100-150 msec: F (1, 16)= 14.09, P <
0.02; 150-200 msec: F (1, 16) = 16.72, P < 0.001; 200-
250 msec ( F (1, 16)= 17.82, P < 0.001) and, further,
that there were no significant group differences in its
amplitude. However, at posterior scalp sites, a promi-
nent negativity was elicited by unattended-ear deviant
tones in the blind but not in the sighted, as shown by
the difference waves in Fig. 2. Analyses of variance for
difference-wave amplitudes at occipital electrodes
(TOc, Oc, Oz, Oi, TOi; see Fig. 2, bottom) indicated a
significant group difference at 200-250 msec (F (1,
16) = 6.63, P < 0.025), where the mean amplitudes at
Oz were - 1 . 3 / z V for the blind and + 0.6/xV for the
sighted. The posterior scalp distribution of the

ERPs TO ATTENDED TONES

....... S T A N D A R D
DEVIANT
BLIND GHTED
HEOGi ~ HEOGc

FCi
Fz- "F
Cc."
\
Ti " Tc .. _ ~
.

\ /

0 300ms

DIFFERENCE: DEV-STAND
- - BLIND
....... S I G H T E D

Fig. 3. Top: grand-average ERPs in the blind and sighted to standard tones (dashed lines) and deviant tones (targets; solid lines) of attended
stimulus sequence. (For further details, see Fig. 1.) Bottom: difference waves for the blind (solid lines) and sighted (dashed lines) groups formed
by subtracting the grand-average ERPs to standard tones of attended stimulus sequence from the ERPs to deviant tones of the same sequence.
424
deviant-tone negativity in the blind was confirmed by a
significant Group × Electrode interaction at 200-250
msec ( F (4, 6 4 ) = 3.66, P < 0.04) in an analysis of
variance (factors: Group, Ear, Electrode) for normal-
ized difference-wave amplitudes at the midline (Fpz,
Fz, Cz, Pz, Oz).
Furthermore, the negativity to unattended-ear de-
viant tones tended to be larger in the blind than
sighted at lateral scalp sites over the auditory cortex
(Fig. 2, bottom), although this effect, tested at elec-
trodes FCc, TCc, Mc, FCi, Ti, and Mi, did not quite
reach statistical significance (200-250 msec: F (1, 16)
= 3.95, P < 0.065). This group difference was larger
over the hemisphere contralateral (electrodes FCc, Tc,
Mc) than ipsilateral (FCi, Ti, Mi) to the stimulated ear,
as indicated by a significant Group x Hemisphere in-
teraction (200-250 msec: F (1, 16) = 5.05, P < 0.04;
250-300 msec: F (1, 16) = 7.08, P < 0.02). However,
the hemispheric asymmetry may have been caused by
small, unrejected (see Methods) eye movement arti-
facts in the blind seen in Fig. 2 especially in H E O G
channels used for monitoring horizontal eye move-
ments.
Interestingly, at latencies shorter than 200 msec the
negativity to unattended-ear deviant tones tended to
reverse its polarity at the mastoid electrodes (Mc and
Mi), as indicated by a positivity in deviant-standard
difference waves at these electrode sites (Fig. 2, bot-
tom). At longer latencies, a negativity was observed at
the mastoids in the blind but not in the sighted.
As seen in Fig. 2, the negativity to unattended-ear
deviant tones was followed by the onset of a P3 positiv-
ity. This P3 was larger in the blind than in the sighted
over frontal and central, but not over posterior, scalp
sites. This difference in the P3 scalp distribution was
confirmed by an analysis of variance for normalized
difference-wave amplitudes at the midline (Fpz, Fz, Cz,
Pz, Oz) at 300-350 msec ( F (4, 6 4 ) = 3.11, P < 0.05).
Unfortunately, a more detailed examination of P3 am-
plitude and peak latency was not possible because in
many subjects, P3 did not peak during the post-stimu-
lus analysis period of 370 msec.
Fig. 3 presents ERPs to standard and deviant (target)
tones and deviant-standard difference waves for the
attended ear. These difference waves show a small
deviant-tone negativity followed by a large P3 deflec-
tion. In the sighted, P3 was largest at posterior scalp
sites, whereas in the blind, P3 was widely distributed
and had large amplitudes even at anterior scalp sites.
This group difference in the P3 distribution was con-
firmed by an analysis of variance for normalized differ-
ence wave amplitudes at the midline (Fpz, Fz, Cz, Pz,
Oz) at 300-350 msec ( F (4, 64) = 3.09, P < 0.05). Again,
P3 could not be studied in more detail, because of the
370 msec analysis period which was too short for this
purpose.
K. ALHO ET AL.
The negativity preceding the P3 to deviant tones was
small (Fig. 3, bottom) and did not reach statistical
significance in either group at any electrode. Further-
more, no significant group difference in the amplitude
of this negativity was found, although it tended to be
larger in the blind than sighted (Cz, 150-200 msec:
blind - 1 . 6 pN; sighted +0.9 ~V; F (1, 16)=2.53,
P < 0.14). As revealed by Fig. 3, the small amplitude of
this negativity may have been caused in both groups by
an overlap of an early P3 onset.
Discussion
The present results show that in the early blind
subjects, the processing negativity (PN) elicited by at-
tended tones had a scalp distribution posterior to that
in the sighted controls. In the blind subjects, a large
PN was even observed at occipital scalp sites (Fig. 1,
bottom), suggesting that their PN might get a contribu-
tion, in addition to auditory and possibly frontal cor-
tices (N~i~it~inen and Michie 1979; N~it~inen t982, 1990;
Giard et al. 1988), from occipital or parietal cortices
which normally participate in visual processing. Fur-
thermore, this group difference in the PN scalp distri-
bution was observed over a wide latency range (100-350
msec from stimulus). Thus, in the blind, both the
earlier and later auditory PN components may be in
part generated in the posterior brain areas. Also a
recent dichotic selective-attention study by Simpson
and his colleagues (G.V. Simpson, Albert Einstein Col-
lege of Medicine, personal communication, March
1992) suggests that in congenitally blind subjects, PN
has a scalp distribution posterior to that in sighted
controls.
In the present study, blindness had also other ef-
fects on the ERPs to standard tones. Both for the
attended and unattended standard tones, the ERPs in
the blind were significantly more positive than those in
the sighted (Fig. 1, top) at 100-200 msec from stimulus
onset (for unattended standard tones, this effect was
seen even at 50-100 msec). An enhancement of the
exogenous P2 component in the blind might contribute
to this positivity, especially at 150-200 msec (cf.,
Niemeyer and Starlinger 1981; Woods et al. 1985), but
cannot solely account for it because it was significant
also at shorter latencies. Because this positivity was
elicited both by the attended and unattended standard
tones and because no significant effects of blindness on
the midline distributions of attended-standard or unat-
tended-standard ERPs were observed at the latencies
where this positivity was significant (50-200 msec from
stimulus onset), this positivity cannot explain the poste-
rior distribution of the attended-unattended difference
waves in the blind (Fig. 1, bottom). However, at longer
AUDITORY ERPs IN BLIND
latencies there was a significant effect of blindness on
the midline distribution of ERPs to the attended stan-
dard tones but not on the distribution of ERPs to the
unattended standard tones. Also, these findings sup-
port the present proposal that, in the blind, the poste-
rior distribution of the negativity indicated by the at-
tended-unattended difference waves was indeed caused
by a posteriorly distributed PN elicited by the attended
stimuli.
Deviant tones occurring in the unattended stimulus
sequence elicited negatively displaced ERPs in relation
to standard-tone ERPs (Fig. 2). In the sighted, this
effect was largest at frontal scalp sites and was presum-
ably caused by the mismatch negativity (MMN) elicited
by deviant tones (N~i~it~inen et al. 1978). In the blind,
the negativity to unattended-ear deviant tones was of
considerable size also over posterior scalp sites (Fig. 2,
bottom). This suggests that in them, posterior brain
areas normally involved in vision might participate in
detecting changes occurring in an unattended auditory
input.
In the blind, the negativity to unattended-ear de-
viant tones tended to be enhanced also at lateral scalp
sites (Fig. 2, bottom). This suggests that early blindness
might enhance processing of auditory stimulus changes
also in auditory cortex. Although artifacts caused by
small (unrejected; see Methods) horizontal eye move-
ments in the blind may have contributed to this group
difference they cannot account for the whole differ-
ence, because the group difference was present even
over the hemisphere ipsilateral to the stimulated ear,
where the eye movement artifact of the blind caused a
positivity (Fig. 2, bottom). Furthermore, potentials
caused by eye movements are strongly attenuated at
long distances from the eyes (e.g., Hillyard and Galam-
bos 1970) and cannot therefore explain the enhanced
negativity to unattended-ear deviant tones in the poste-
rior scalp areas of the blind.
In the blind, the posterior negativity to the unat-
tended-ear deviant tones peaked later than the frontally
recorded MMN to these tones (Fig. 2, bottom). This
posterior negativity coincided with a negativity which
was observed in the blind at the temporal scalp sites
and which did not invert in polarity at the mastoids.
The polarity reversal of MMN observed in both groups
at shorter latencies is consistent with the previous
findings suggesting that the MMN partly originates
from supratemporal auditory cortex (e.g., Hari et al.
1984; Alho et al. 1986a; Scherg et al. 1989; Javitt et al.
1991; Paavilainen et al. 1991). However, MMN proba-
bly also has a frontal subcomponent (Giard et al. 1990)
and might even have a subcomponent generated in the
auditory association areas on the lateral surface of the
temporal lobe (Paavilainen et al. 1991). The deviant-
tone negativity observed in the blind over the temporal
scalp might be the temporal MMN subcomponent of
425
Paavilainen et al. (1991). Judging from its large ampli-
tudes at posterior scalp sites, parietal or occipital brain
areas might also contribute to this MMN subcompo-
nent in the blind.
Another possibility is that the posterior distribution
of the deviant-tone negativity in the blind was caused
by a posteriorly distributed N2b component overlap-
ping with the MMN. In normal subjects, MMN is
usually followed and partly overlapped by the N2b
component in ERPs to deviant stimuli occurring in an
attended stimulus sequence (NS~it~nen et al. 1982; Sams
et al. 1985, 1990; Alho et al. 1990; N~i~itSnen 1990;
Novak et al. 1990). In a parallel experiment (Kujala et
al. 1992), the N2b component elicited in early blind
subjects by deviant stimuli in an auditory discrimina-
tion task appeared to be distributed posteriorly to that
of sighted controls. Simpson and his colleagues (G.V.
Simpson, Albert Einstein College of Medicine, per-
sonal communication, March 1992) have recently ob-
tained similar results. If the present posterior distribu-
tion of the negativity elicited by unattended-ear de-
viant tones in the blind was indeed caused by a posteri-
orly distributed N2b component overlapping with the
MMN, this might indicate that changes in unattended
auditory stimuli cause an attention shift, and therefore
elicit the N2b more easily in the blind than in the
sighted. Low thresholds for involuntary orienting of
attention may have developed in the blind because of
their increased dependence on auditory stimuli.
Unfortunately, in the present study, the effects of
early blindness on MMN and N2b to target stimuli in
the attended input were difficult to estimate because
P3 components apparently overlapped with these nega-
tive components in the target ERPs (Fig. 3). Interest-
ingly, in these ERPs, as well as in the ERPs to unat-
tended-ear deviant tones (Fig. 2), P3 was more frontally
distributed in the blind than in the sighted. This sug-
gests a larger fronto-centrally dominant P3a compo-
nent (Squires et al. 1975; N~i~it~inenet al. 1982; Sams et
al. 1985) in the blind. Also this finding might be related
to enhanced orienting to auditory stimulus changes in
the blind.
Magnetic resonance imaging (MRI) and positron
emission tomography (PET) have indicated no
macroanatomical or functional degeneration of occipi-
tal cortex in the early blind (Phelps et al. 1981; Wanet-
Defalque et al. 1988). These findings contradict the
possibility that degeneration of occipital cortex in the
blind had changed the orientation of ERP sources in
auditory cortex so that this would have resulted in
large PN and MMN (or N2b) amplitudes at posterior
scalp areas. This possibility is also contradicted by the
present result that the N1 deflection (mainly originat-
ing from auditory cortex at a high stimulation rate;
N~i~it~inen and Picton 1987) was similarly distributed
over the scalp in the blind and sighted.
426
In conclusion, the present data, together with previ-
ous ERP studies of early sensory deprivation in hu-
mans (Niemeyer and Starlinger 1981; Neville et al.
1983; Woods et al. 1985; Neville and Lawson 1987; Uhl
et al. 1991; Kujala et al. 1992), show that plastic changes
occurring in non-deprived modalities may be studied
with scalp-recorded ERPs. The present ERP data sug-
gest that cortical areas normally involved in vision
might participate in auditory selective and involuntary
attention in the early blind. Further research with
more elaborated methods for localizing cortical sources
of ERPs associated with auditory processing (cf., Hari
et al. 1984, 1989; Giard et al. 1988, 1990; Scherg et al.
1989) is needed to confirm that the posterior scalp
distributions of PN and the deviant-tone negativity
(MMN or N2b) observed in the early blind are indeed
caused by an involvement of occipital or parietal corti-
cal areas in auditory processing.
References
Alho, K. Selective attention in auditory processing as reflected by
event-related brain potentials. Psychophysiology, 1992, 29: 247-
263.
Alho, K., Paavilainen, P., Reinikainen, K., Sams, M. and Nhhthnen,
R. Separability of different negative components of the event-re-
lated brain potential associated with auditory stimulus processing.
Psychophysiology, 1986a, 23: 613-623.
Alho, K., Sams, M., Paavilainen, P. and Niiiit~inen, R. Small pitch
separation and the selective-attention effect on the ERP. Psy-
chophysiology, 1986b, 23: 186-197.
Alho, K., Donauer, N., Paavilainen, P., Reinikainen, K., Sams, M.
and Nhhthnen, R. Stimulus selection during auditory spatial
attention as expressed by event-related potentials. Biol. Psychol.,
1987a, 24: 153-162.
Alho, K., T6tt61ii, K., Reinikainen, K., Sams, M. and N~iiit~inen, R.
Brain mechanisms of selective listening reflected by event-related
potentials. Electroenceph. clin. Neurophysiol., 1987b, 68: 458-
470.
Alho, K., Sams, M., Paavilainen, P., Reinikainen, K. and Nhhthnen,
R. Event-related brain potentials reflecting processing of relevant
and irrelevant stimuli during selective listening. Psychophysiology,
1989, 26: 514-528.
Alho, K., Lavikainen, J., Reinikainen, K., Sams, M. and Niiiithnen,
R. Event-related brain potentials in selective listening to frequent
and rare stimuli. Psychophysiology, 1990, 27: 73-86.
Alho, K., Woods, D.L., Algazi, A. and Nhhthnen, R. lntermodal
selective attention. II. Effects of attentional load on processing of
auditory and visual stimuli in central space. Electroenceph. olin.
Neurophysiol., 1992, 82: 356-368.
Carlson, S., Pertovaara, A. and Tanila, H. Late effects of early
binocular visual deprivation on the function of Brodmann's area
7 of monkeys (Macaca arctoides). Dev. Brain Res., 1987, 33:
101-111.
Dehay, C., Kennedy, H. and Bullier, J. Characterization of transient
cortical projections from auditory, somatosensory, and motor
cortices to visual areas 17, 18, and 19 in the kitten. J. Comp.
Neurol., 1988, 272: 68-89.
Dixon, W.J., Brown, M.B., Engelman, L., Hill, M.A. and Jennrich,
R.I. (Eds.). BMDP Statistical Software Manual. University of
California Press, Berkeley, CA, 1988.
K. ALHO ET AL.
Giard, M.H., Perrin, F., Pernier, J. and Peronnet, F. Several atten-
tion-related wave forms in auditory areas: a topographic study.
Electroenceph. din. Neurophysiol., 1988, 69: 371-384.
Giard, M.H., Perrin, F., Pernier, J. and Bouchet, P. Brain generators
implicated in the processing of auditory stimulus deviance: a
topographic ERP study. Psychophysiology, 1990, 27: 627-640.
Hari, R., H~im~iliiinen, M., Ilmoniemi, R., Kaukoranta, E.,
Reinikainen, K., Salminen, J., Alho, K., Niiiitiinen, R. and Sams,
M. Responses of the primary auditory cortex to pitch changes in
a sequence of tone pips: neuromagnetic recordings in man. Neu-
rosci. Lett., 1984, 50: 127-132.
Hari, R., Hiimiil~iinen, M., Kaukoranta, E., Miikelii, J., Joutsiniemi,
S.L. and Tiihonen, J. Selective listening modifies activity of the
human auditory cortex. Exp. Brain Res., 1989, 74: 463-470.
Hillyard, S.A. and Galambos, R. Eye movement artifact in the CNV.
Electroenceph. clin. Neurophysiol., 1970, 28: 173-182.
Hyv~irinen, J., Carlson, S. and Hyv§rinen, L. Early visual deprivation
alters modality of neuronal responses in area 19 of monkey
cortex. Neurosci. Lett., 1981a, 26: 239-243.
Hyvhrinen, J., Hyv~irinen, L. and Linnankoski, I. Modification of
parietal association cortex and functional blindness after binocu-
lar deprivation in young monkeYs. Exp. Brain Res., 1981b, 42:
1-8.
Javitt, D.C., Schroeder, C.E., Arezzo, J. and Vaughan, Jr., H.G.
Selective inhibition of "processing-contingent" auditory event-re-
lated potentials by the phencyclidine (PCP)-like agent MK-801.
Electroenceph. clin. Neuropbysiol., 1989, 79: 65P.
Kujala, T., Alho, K., Paavilainen, P., Summala, H. and Niihtiinen, R.
Neural plasticity in processing sound location by the early blind:
an event-related potential study. Electroenceph. clin. Neurophys-
iol., 1992, 84: 469-472.
Kujala, T., Kekoni, J., Reinikainen, K., Hhmiihiinen, H., N'ahthnen,
R. and Alho, K. Auditory and somatosensory processing in the
early blind. 1993, in preparation.
McCarthy, G. and Wood, C.C. Scalp distributions of event-related
potentials: an ambiguity associated with analysis of variance mod-
els. Electroenceph. clin. Neurophysiol., 1985, 62: 203-208.
Merzenich, M.M., Jenkins, W.M. and Middlebrooks, J.C. Observa-
tions and hypotheses on special organizational features of the
central auditory nervous system. In: G.M. Edelman, W.E. Gall
and W.M. Cowan (Eds.), Dynamic Aspects of Neocortical Func-
tion. Wiley, New York, 1984: 397-424.
Nh~thnen, R. Processing negativity: an ew~ked-potential reflection of
selective attention. Psychol. Bull., 1982, 92: 605-640.
Nhhthnen, R. The role of attention in auditory information process-
ing as revealed by event-related brain potentials. Behav. Brain
Sci., 1990, 13: 201-288.
Nh~ithnen, R. Mismatch negativity (MMN) outside strong attentional
focus: a commentary on Woldorff et al. (1991). Psychophysiology,
1991, 28: 478-484.
Nii~ithnen, R. Attention and Brain Function. Erlbaum, New York,
1992.
N~i~thnen, R. and Gaillard, A.W.K. The orienting reflex and the N2
deflection of the ERP. In: A.W.K. Gaillard and W. Ritter (Eds.),
Tutorials in Event-Related Potential Research: Endogenous
Components. North-Holland Publ, Amsterdam, 1983: 119-114.
N~i~ithnen, R. and Michie, P.T. Early selective-attention effect on the
evoked potential. A critical review and reinterpretation. Biol.
Psychol., 1979, 8: 81-136.
Nhhthnen, R. and Picton, T.W. The N1 wave of the human electric
and magnetic response to sound: a review and an analysis of
component structure. Psychophysiology, 1987, 24: 375-425.
Nhhthnen, R., Gaillard, A.W.K. and M~intysalo, S. Early selective-at-
tention effect on evoked potential reinterpreted. Acta Psychol.
(Amst.), 1978, 42: 313-329.
Nh~ithnen, R., Simpson, M. and Loveless, N.E. Stimulus deviance
and evoked potentials. Biol. Psychol., 1982, 14: 53-98.
AUDITORY ERPs IN BLIND
N~i~it~inen, R., Sams, M. and Alho, K. The mismatch negativity: the
ERP sign of a cerebral mismatch process. In: W.C. McCallum, R.
Zappoli and F. Denoth (Eds.), Cerebral Psychophysiology. Elec-
troenceph, clin. Neurophysiol, Suppl. 38. Elsevier, Amsterdam,
1986: 172-178.
Neville, H.J. and Lawson, D. Attention to central and peripheral
visual space in a movement detection task: an event-related
potential and behavioral study. II. Congenitally deaf adults. Brain
Res., 1987, 405: 268-283.
Neville, H.J., Schmidt, A. and Kutas, M. Altered visual-evoked
potentials in congenitally deaf adults. Brain Res., 1983, 226:
127-132.
Niemeyer, W. and Starlinger, I. Do the blind hear better? Investiga-
tions on auditory processing in congenital or early acquired
blindness. II. Central functions. Audiology, 1981, 20: 510-515.
Novak, G.P., Ritter, W., Vaughan, Jr., H.G. and Wiznitzer, M.L.
Differentiation of negative event-related potentials in an auditory
discrimination task. Electroenceph. clin. Neurophysiol., 1990, 75:
255-275.
Paavilainen, P., Alho, K., Reinikainen, K., Sams, M. and Nii~it~inen,
R. Right-hemisphere dominance of different mismatch negativi-
ties. Electroenceph. clin. Neurophysiol., 1990, 78: 466-479.
Parasuraman, R. Effects of information processing demands on slow
negative shift latencies and N100 amplitude in selective and
divided attention. Biol. Psychol., 1980, 11: 217-233.
Phelps, M.E., Mazziota, J.C., Kuhl, D.E., Nuwer, M., Packwood, J.,
Metter, J. and Engel, J. Tomographic mapping of human cerebral
metabolism: visual stimulation and deprivation. Neurology, 1981,
31: 512-529.
Rebillard, G., Carlier, E., Rebillard, M. and Pujol, R. Enhancement
of visual responses in the primary auditory cortex of the cat after
an early destruction of cochlear receptors. Brain Res., 1977, 129:
162-164.
Ryugo, D.K., Ryugo, R., Globus, A. and Killackey, H.P. Increased
427
spine density in auditory cortex following visual or somatic deaf-
ferentation. Brain Res., 1975, 90: 143-146.
Sams, M., Paavilainen, P., Alho, K. and N~i~it~inen, R. Auditory
frequency discrimination and event-related potentials. Electroen-
ceph. clin. Neurophysiol., 1985, 62: 437-448.
Sams, M., Aulanko, R., Aaltonen, O. and N~it~inen, R. Event-re-
lated potentials to infrequent changes in synthesized phonetic
stimuli. J. Cogn. Neurosci., 1990, 2: 344-357.
Scherg, M., Vajsar, J. and Picton, T. A source analysis of the human
auditory evoked potentials. J. Cogn. Neurosci., 1989, 1: 336-355.
Squires, N.K., Squires, K.C. and Hillyard. S.A. Two varieties of
long-latency positive waves evoked by unpredictable auditory
stimuli in man. Electroenceph. clin. Neurophysiol., 1975, 38:
387-401.
Strelow, E.R. and Brabyn, J.A. Locomotion of the blind controlled
by natural sound cues. Perception, 1982, 11: 635-640.
Uhl, F., Franzen, P., Lindinger, W., Lang, W. and Deecke, L. On the
functionality of the visually deprived occipital cortex in early
blind persons. Neurosci. Lett., 1991, 124: 256-259.
Wanet-Defalque, M.C., Veraart, C., De Voider, A., Metz, R., Michel,
C., Dooms, G. and Goffinet, A. High metabolic activity in the
visual cortex of early blind human subjects. Brain Res., 1988, 446:
369-373.
Woldorff, M., Hackley, S.A. and Hillyard, S.A. The effects of chan-
nel-selective attention on the mismatch negativity wave elicited
by deviant tones. Psychophysiology, 199l. 28: 30-42.
Woods, D.L., Clayworth, C.C. and Bach-y-Rita, P. Early blindness
reorganizes auditory processing in humans. In: Abstracts, Society
for Neuroscience, 15th Annual Meeting, Dallas TX, Oct. 20-25,
1985: 449.
Woods, D.L., Alho, K. and Algazi, A. Intermodal selective attention.
I. Effects on event-related potentials to lateralized auditory and
visual stimuli. Electroenceph. clin. Neurophysiol., 1992, 82: 341-
355.