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Binaural interaction (BI) is known to occur Huang 1975; Huang and Buchwald 1977;
at most levels of the auditory brain stem: Stockard and Rossiter 1977). Waves I and II
inferior colliculus {Erulkar 1959; Hind et al. almost certainly represent synchronous dis-
1963; Lehman and Hafter 1972), dorsal nu- charge of units in the VIIIth nerve and
cleus of the lateral lemniscus (Brugge et al. cochlear nuclei, respectively, ipsilateral to the
1970), superior olivary complex (Galambos et ear stimulated. Later waves presumably repre-
al. 1959; Hall 1965), and dorsal cochlear nu- sent activity at higher levels: superior olivary
cleus {Mast 1970). Psychophysical tests of BI, complex, nuclei of the lateral lemnisci, infe-
including phase audiometry (Nilsson et al. rior colliculi, and medial geniculate. The pre-
1973), localization tests (Jerger 1960a, b; cise identification of the sources of later
Matzger 1959), and the masking level differ- waves is unclear; third and higher order units
ence test (Olsen et al. 1976), are sensitive to are dispersed throughout the auditory brain
lesions affecting the brain stem in man. Simi- stem, and it is likely that multiple generators,
lar effects have been seen in behavioral studies including both the brain stem nuclei and asso-
in animals after experimental brain stem ciated fiber tracts, are involved (Achor 1976).
lesions (Masterton et al. 1967, 1968; Casseday Since BI is prominent in the unit activity
and Neff 1975). recorded from brain stem auditory units, it
A physiological test of BI has potential seemed appropriate to study this phenome-
value in the clinical evaluation of patients non in far-field surface recorded potentials,
with suspected disorders of the central audi- such as BSEP.
tory nervous system. In recent years, the Dobie and Berlin (1979) studied BI in the
brain stem evoked potential (BSEP) has been BSEP of anesthetized guinea pigs. BI was
widely used in the study of both normal and defined as any deviation from the predictions
abnormal auditory systems. BSEP appears to of a simple monaural-addition model of bin-
reflect the volume-conducted algebraic sum of aural responses. Such a model assumes two
neural activity of large numbers of neurons in independent BSEP generators (or sets of
the brain stem auditory nuclei (Buchwald and generators), one for each ear, whose outputs
do not interact. System o u t p u t under condi-
tions of binaural stimulation would then be
1 This study was supported by PHS Fellowship Grant pre~lictable by algebraic summation of the
No. NS-07058-01A1 and by a Veterans Administra- responses to monaural stimulation. In practice,
tion Research Advisory Group grant. for a given stimulus condition, responses to
2 Correspondence to: Robert A. Dobie, M.D.,
F.A.C.S., Chief, Otolaryngology, VA Medical Center,
binaural, right, and left stimulation are
4435 Beacon Avenue South, Seattle, Wash. 98108, recorded. The left and right monaurally
U.S.A. evoked responses are added together to yield
304 R.A. D O B I E , S.J. N O R T O N
Ill
IL
I i1~ IV V
IV
DP2
DN I llO pV
I
1 msec
Fig. 1. B i n a u r a l i n t e r a c t i o n in g u i n e a pig BSEP. L e f t : r e s p o n s e s f r o m m o n a u r a l (L, R) a n d b i n a u r a l (B) stimula-
t i o n . R i g h t : b i n a u r a l r e s p o n s e t h a t w o u l d be p r e d i c t e d b y s u m m a t i o n o f t h e m o n a u r a l r e s p o n s e s (P = L + R),
c o m p a r i s o n o f t h e B a n d P traces, a n d t h e d i f f e r e n c e trace (D = B - - P) r e p r e s e n t i n g derived b i n a u r a l i n t e r a c t i o n .
S t i m u l u s i n t e n s i t y = 87 dB p e S P L ; 20 clicks/sec; N = 512. C o m p a r a b l e d a t a f r o m a h u m a n s u b j e c t are s h o w n in
Fig. 3.
the model's predicted binaural response (the P about 3.5--4.0 msec) there was significant
trace), and this is compared to the obtained non-linear interaction as reflected in the am-
binaural response (the B trace). plitude of wave IV and the latency of peak
In addition, a difference trace (D) is ob- IV' (the vertex-negative peak following wave
tained by subtracting the P trace from the B IV}. Both are significantly reduced in the bin-
trace. In the absence of BI, the result will be a aural condition. The D traces were character-
straight line, D = 0. With this technique, inter- ized by a sharp negative peak followed by a
action occurring anywhere in the response positive peak with latencies roughly corre-
will be seen in the D trace; comparison of sponding to waves IV and IV', respectively.
peak amplitudes and latencies in the B and P The BI as reflected in the D trace was of a
traces could miss interactions at points other greater magnitude and complexity than that
than the wave peaks. indicated by direct comparison of wave IV
The basic paradigm is illustrated in Fig. 1. and IV' in the B and P conditions. BI was
The interaction was similar for all animals maximal for simultaneous clicks of equal
tested. There was no interaction in waves I intensity, but was present in a majority of ani-
through III. In the wave IV region {latency of mals when interaural time differences of up to
BINAURAL INTERACTION IN EVOKED POTENTIALS 305
y-
FREQUENCY (KHz) Data analysis was carried o u t after off-line
averaging of the responses. For each condi-
tion, the dependent variables were the ampli-
tudes and latencies of response peaks. For
BSEP, the vertex positive peaks II through VI
and the subsequent vertex negative peaks
(arbitrarily .named II' through VI', omitting
the negative peak between IV and V which is
often absent) were measured; for middle AEP,
the peaks selected for measurement were
those conventionally labeled No, Po, Na, Pa,
and Nb (Goldstein and R o d m a n 1967). For
each set of 3 stimulus blocks, in addition to
the measurement of peaks in the raw traces, a
derived trace (P) was generated b y summing
I I the appropriate monaural responses; its peaks
O. 5 m sec were measured in the same way. For BSEP,
Fig. 2. Above: spectrum o f stimulus, as transduced by the peaks in the difference trace (D = B -- P)
TDH-49 earphone. Peak energy is at 3640 Hz. Below: were also measured. Analysis of variance was
acoustic wave form of stimulus for right and left ear- carried out for each dependent variable, i.e.,
phones; a downward deflection indicates rarefaction. the amplitudes and latencies of each response
peak. The first analysis performed compared
monaural responses, i.e., right versus left. No
FM channel was used. Filter slopes were 6 dB/ significant differences were found, and these
octave. The nominal frequency response of data will not be presented. The second anal-
the tape deck at 3.75 in./sec was 50--15,000 ysis of variance compared the B and the P
Hz for direct mode and 0--1250 Hz for FM conditions as well as any differences between
mode. Both the ongoing filtered EEG activity the first and second replication at the high
and the running averaged BSEPs were moni- intensity level. No order effects were found
tored during each experiment, b u t all data and the data from the t w o replications were
analysis was performed by reaveraging the collapsed for purposes of calculating the
data from tape off-line. For BSEP, dwell time group means and standard errors which are
was 40 #sec; for middle AEP, dwell time was plotted in the ensuing figures. N o t all peaks
280/~sec. were measurable in every trace. However,
BINAURAL INTERACTION IN EVOKED POTENTIALS 307
Results
.13Z - ' ~
STIM
ART Tr TIT [
Io.5~v
0 251~V
I m sec
P,
the D trace was reminiscent of that seen in
Io.25/~v guinea pig BSEP (Fig. 1), and the response
peaks have been similarly named. However,
the first negative peak (NI) occurred later in
Nt
the human response; its latency was about 6.0
msec compared to 3.5--4.0 msec in the guinea
1 I pig. Inspection of the D traces for all 16 sub-
I rn s e c jects (Fig. 4) revealed that most showed
Fig. 3. Binaural interaction in h u m a n BSEP. Sum of responses of the same general type. Although
monaural responses (P) compared to binaurally there was considerable individual variability,
evoked responses (B). Difference trace (D) calculated 28 of the 32 traces (in 15 of 16 subjects)
by subtracting P from B (note different scale for showed an identifiable N1 whose latency, for
response amplitude). Stimuli were 0.1 msee clicks at
97 dB peSPL (high-intensity condition), 10/sec, N = a given subject, always was intermediate
2048 for each of two replications for each condition. between the latencies of peaks V and V' in
'Stim Art' = stimulus artifact. the B trace.
308 R.A. DOBIE, S.J. NORTON
4-
,3--
]I ~ " .3-
.2-- ! p, '. .2-
.t- 3-
O- 0-
:l-- N2
>
--.P_-- ~-~-:2 -
]K' N,3-
0 PREDICTED
[ ] PREDICTE0
• BINAUflAL
=5- • BINAURAL g-15-
~--.6-- DtFFERENCE
DIFFERENCE
117-- LOW INTEN~TY / B.5.E.P.
< :7- HIGH INTENISCTYIB.S.E.P.
-18- --'8--
<9- --19--
-LO - --fO --
-LI-
-12 -
-15 - ,~ 2.% 3'.0 .Io ~o ~ ~'o ~o 9:0
LATENCY (rn sec}
LATENCY tm sec)
Fig. 6. Group mean amplitudes and latencies for bin-
Fig. 5. Group mean amplitudes and latencies for bin- aural, predicted and difference traces in the low-
aurally evoked BSEP (binaural), the sum of the mon- intensity BSEP condition (N = 7).
aurally evoked responses (predicted), and the differ-
ence trace in the high-intensity condition (N -- 16).
Peak-labeling convention is as seen in Fig. 3. The p e a k N2 w a s identifiable in o n l y 20 o f 32
height of each rectangle represents twice the standard traces.
error of the mean for response amplitude; the width G r o u p data for t h e 7 subjects w h o r e c e i v e d
represents twice the S.E.M. for latency. Mean ampli- t h e l o w i n t e n s i t y clicks as well are s h o w n in
tude and latency for each response peak is at the cen- Fig. 6. There w a s a generalized decrease in
ter of the appropriate rectangle.
P0
P e a k a m p l i t u d e s a n d l a t e n c i e s for t h e B a n d
P traces, in t h e h i g h - i n t e n s i t y c o n d i t i o n , are
s h o w n in Fig. 5. E a c h p e a k is r e p r e s e n t e d b y a
P° I o.2 v
rectangle w h o s e c e n t e r r e p r e s e n t s t h e g r o u p
m e a n for a m p l i t u d e and l a t e n c y . T h e h e i g h t
a n d w i d t h o f t h e r e c t a n g l e s represent standard
errors o f :the m e a n s f o r a m p l i t u d e s and laten-
N0 Nb
cies, r e s p e c t i v e l y . It can be seen by inspec-
t i o n , and w a s c o n f i r m e d in t h e analysis o f
variance, t h a t t h e r e w e r e n o significant differ-
e n c e s (P > 0 . 0 5 ) b e t w e e n t h e peak values for
t h e B and P traces. T h e r e is a s u g g e s t i o n o f
D
slightly earlier latencies in t h e B trace for all
p e a k s after p e a k IV, b u t n o n e o f t h e s e differ-
e n c e s w a s individually significant.
T h e m e a n data for t h e p e a k s in t h e D trace
are p l o t t e d in t h e s a m e figure, N o t e that t h e l l
p e a k d i f f e r e n c e s o c c u r w i t h latencies w h i c h 5 m sec
are in every case i n t e r m e d i a t e b e t w e e n t h o s e
Fig. 7. Binaural interaction in h u m a n middle-latency
o f t h e r e s p o n s e p e a k s in t h e r a w B S E P traces. auditory evoked potentials, in the high-intensity con-
P e a k s P1 and N1 w e r e e a c h identifiable in 2 8 dition. Response labeling (B, P, D) and stimulus
o f 32 D traces; p e a k P2 w a s s e e n in 2 7 , w h i l e parameters are as described for Fig. 3.
BINAURAL INTERACTION IN EVOKED POTENTIALS 309
~ P
B
p5
I0
/
P.
x\\ \
0 PR~OPCTEO
• B4N~U"AL
HIGH PP~TgNSIT¥
I
I,~v
''\ ' "
:
' 2 / \ 1
" \\
I I
I 0 m sec
-2o 1."
Fig. 8. Binaural interaction typical of that seen in 4 T } T I ~ I I I I I I T
~ T I i0 I ~ 2[0 ~0 I I I ~ U ]
subjects with middle-latency responses thought to be
LATENCY (m sec)
myogenic (see text). Note large amplitude (>8 pV)
and early latency (15--20 msec) of presumed myo-
Fig. 9. Group mean amplitudes and latencies for bin-
genic response.
aural, predicted and difference traces in the high-
intensity middle-latency response condition (N = 12).
Peak-labeling convention is as seen in Fig. 7.
2.0
rl
is not necessarily attributable to interaction at
1.5 j P~ / / ~ [] PRE~CTEO a higher site; this could represent third-order
(or higher) activity at any level central to the
1.0 :
.5-
i/il MID~)LE A.E.P.
cochlear nuclei.
Parametric differences (particularly in stim-
ulus spectrum) may also explain some of this
LU O"
difference. Broad-band clicks delivered to
d_:5- TDH-49 earphones were used in both experi-
:
-I.0 : ments, b u t the stereotaxic ear bar system used
N No N= to couple the sound source to the guinea pig's
-15
ear canal introduced large tube resonances at
-2.0 approximately 750 and 1500 Hz. This was a
f I l I I f I I I I I I I I [ I I I I I I I l I considerably different spectrum than that
ro 20 30 40
LATENCY (m sec) delivered to the human subjects. It is possible
that the degree of BI seen in BSEP is a func-
Fig. 10. Group mean amplitudes and latencies for bin- tion of stimulus spectrum; this hypothesis is
aural, predicted and difference traces in the low- being studied currently in our laboratory.
intensity middle-latency response condition (N = 6).
In humans, the peak measurements of bin-
aurally evoked BSEP are accurately predicted
by simple summation of monaural responses.
Discussion In the group mean data, there were no signifi-
cant differences for amplitude or latency for
BI similar to that seen in the guinea pig any of the response peaks in BSEP. The BI
(Dobie and Berlin 1979) was demonstrated in was apparent only when the D traces were
BSEP in the majority of subjects. In humans, examined. The peaks in these D traces (i.e.,
BI occurred later in the response (about the largest differences between the B and P
6 msec) and showed considerably more varia- traces) occurred invariably with latencies
bility than in the guinea pig. There are several which were intermediate between those of the
possible explanations for this. Guinea pig response peaks in the raw BSEP; this is
BSEP amplitudes are typically several pV exactly what one would expect if the interac-
compared to the sub-microvolt levels seen in tion were expressed primarily as a small
humans; this is p r e s u m a b l y because of differ- latency shift.
ences in brain and skull anatomy. Higher sig- BI was also seen in middle AEP. There was
nal-to-noise ratios in guinea pigs lead to no interaction in the early portion of this
'cleaner' responses even when fewer samples response, which presumably reflects the same
are averaged. In addition, the guinea pigs were neural activity seen in the BSEP as filtered
anesthetized, which contributed to the stabil- with a lower bandpass. However, in both the
ity of the recordings. Innate species differ- high- and low-intensity conditions, the ampli-
ences must be considered; the large difference tude of peak Pa in the B trace was consider-
in brain stem size may account for some of ably less than predicted b y summation of the
the latency difference. In addition, if binaural monaural responses. This we interpret as con-
integrative functions in man were attributable sistent with a neural response in which there
to sites which were 'higher' and more distrib- is some overlap of elements responding in the
uted along the ascending auditory pathway left and right monaural conditions.
than in the guinea pig, one might expect to For both BSEP and middle AEP, the pat-
see BI in evoked potentials showing longer terns of BI were identical in the h i g h - a n d
latencies and less coherence. Of course, the low-intensity conditions. This effectively rules
longer latency of the BI potential in humans o u t acoustic crossover as an important arti-
BINAURAL INTERACTION IN EVOKED POTENTIALS 311
fact, since the low-intensity clicks were only 6 msec latency region) was observed in the
a b o u t 35--40 dB above the subjects' thresh- difference trace for the majority of subjects'
olds. BSEP, there were no significant differences
Four subjects showed middle AEPs which between binaural and predicted-binaural
were qualitatively different. These were responses in the group means for individual
believed to be primarily myogenic on the peak amplitudes and latencies.
basis of their latency and amplitude character- In middle AEP, the amplitude of peak Pa
istics. The pattern of BI seen here was also was usually much smaller in binaurally evoked
consistent with a myogenic response near responses than in the predicted-binaural
threshold: small increments in stimulus inten- response. Four subjects had middle AEP
sity (in this case, binaural versus monaural) which were felt to be predominantly myo-
resulted in large increases in response ampli- genic on the basis of short latency and large
tude. A steep growth function is characteristic amplitude; these responses demonstrated a
of the post-auricular myogenic response (Pic- reverse pattern of interaction, with binaural
t o n et al. 1977). In retrospect, a more appro- responses much larger than the monaural
priate site for the reference electrode, to sums.
avoid myogenic potentials, might have been
the anterior neck, over the larynx.
BI is an important aspect of the function of R~sum~
the auditory nervous system at brain stem and
higher levels; in human subjects, BI can be Interaction binaurale duns les potentiels
demonstrated in both BSEP and middle AEP. dvoqugs auditifs
If the problems of individual variability dis-
cussed above can be solved, tests such as these L'interaction binaurale (BI) duns les poten-
could become useful in clinical settings. tiels ~voqu~s auditifs est d~finie c o m m e toute
d~viation des predictions d'un module qui
postule deux populations ind~pendantes de
Summary neurones dont les sorties seraient, ~ distance,
simplement additives. Les r~ponses monau-
Binaural interaction (BI) in auditory rules sont additionn~es pour aboutir ~ la pr~-
evoked potentials was defined as any devia- diction du module de la r~ponse ~voqu~e de
tion from the predictions of a model which fa~on binaurale; cette trace est ensuite sous-
assumes two independent populations of neu- traite de la r~ponse binaurale r~elle pour con-
rons whose o u t p u t s are, in the far field, sim- duire au trac~ d'une difference qui est consi-
ply additive. Monaural responses are added to d~r~e representer la BI. Duns une ~tude ant~-
yield the model's prediction of binaurally rieure, une BI forte a ~t~ observ~e duns le
evoked response; this trace is then subtracted BSEP du cobaye, maximale ~ une latence
from the actual binaural response to yield a d'environ 4 msec: l'interaction est plus grande
difference trace which is considered to repre- pour des stimulus simultan~s {At = 0) d'inten-
sent BI. In a previous study, strong BI was sit~ ~gale (AI = 0).
seen in guinea pig BSEP, maximal at a b o u t Seize jeunes adultes normaux ont ~t~ enre-
4 msec latency; the interaction was greatest for gistr~s en ce qui concerne les BSEP et les
simultaneous (At = 0) stimuli of equal inten- potentiels ~voqu~s auditifs de latence moy-
sity (AI = 0). enne (AEP moyen) en r~ponse ~ des clics
Sixteen normal y o u n g adults had BSEP and binauraux et monauraux. Bien que la BI (duns
middle-latency auditory evoked potentials la zone de latence de 6 msec) soit observ~e
(middle AEP) recorded in response to binau- duns le trac~ de difference duns la majorit~
ral and monaural clicks. Although BI (in the des BSEP des sujets, il n'y a pus de difference
312 R.A. DOBIE, S.J. NORTON
significative entre les r~ponses binaurales et Galambos, R., Schwartzkopf, J. and Rupert, A.
les r~ponses binaurales prddites darts les moy- Microelectrode study of the superior olivary nu-
clei. Amer. J. Physiol., 1959, 197: 527--536.
ennes de groupe en ce qui concerne les ampli-
Gerken, G.M., Moushegian, G., Stillman, R.D. and
tudes et les latences de pics individuelles. Pour Rupert, A.L. Human frequency following
les AEP moyens, l'amplitude du pic Pa est responses to monaural and binaural stimuli. Elec-
habituellement beaucoup plus petite dans les troenceph, clin. Neurophysiol., 1975, 38:
r~ponses ~voqudes de fa~on binaurale que 397--386.
Goldstein, R. and Rodman, L.B. Early components of
dans la r~ponse binaurale pr~dite. Quatre
averaged evoked responses to rapidly repeated
sujets ont des AEP moyens qui sont supposes auditory stimuli. J. Speech Hearing Res., 1967,
~tre de faqon pr~dominante myog~niques sur 10: 697--705.
la base d'une latence courte et d'une ampli- Hall, J. Binaural interaction in the accessory superior
tude dlevde; ces rdponses montrent un mode olivary nucleus of the cat. J. acoust. Soc. Amer.,
inverse d'interaction, les r~ponses binaurales 1965, 37: 814--823.
Hind, J.E., Goldberg, J.M., Greenwood, D.D. and
~tant plus grandes que les sommes des Rose, J.E. Some discharge characteristics of single
rdponses monaurales. neurons in the inferior colliculus of the cat. II.
Timing of the discharges and observations of bin-
We thank Dr. Charles I. Berlin for his advice and aural stimuli. J. Neurophysiol., 1963, 26:
encouragement and Dr. Larry Hughes and Charles 321--341.
Weisendanger for their help with the statistical anal- Huang, C.M. and Buchwald, J.S. Interpretation of the
ysis. Drs. Josef Miller, Jack Cullen, Ted Glattke and vertex short-latency acoustic response: a study of
Craig Wier read earlier drafts of this paper and made single neurons in the brain stem. Brain Res., 1977,
helpful suggestions. The data were collected while the 137: 291--303.
senior author was a post-doctoral fellow at the Kresge Huang, C.M. and Buchwald, J.S. Factors that affect
Hearing Research Laboratory of the South, Louisiana amplitude and latency of vertex short-latency
State University Medical Center, New Orleans, La., acoustic responses in the cat. Electroenceph. clin.
U.S.A. Neurophysiol., 1978, 44: 179--186.
Jerger, J. Audiological manifestations of lesions in the
auditory nervous system. Laryngoscope, 1960a,
70: 417--425.
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BINAURAL INTERACTION IN EVOKED POTENTIALS 313
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