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The Excitatory Process in the Cochlea

Authors:
PHYSIOLOG
Y:
DA
VIS,
ET
AL.
*
Contribution
No.
1442.
t
This
work
was
aided
by
a
research
grant
from
the
National
Heart
Institute,
of
the
National
Institutes
of
Health.
Dr.
Lippman
is
a
Fellow
of
the
John
Simon
Guggen-
heim
Memorial
Foundation.
'Landsteiner,
K.,
The
Specificity
of
Serologial
Reactions,
Harvard
Univ.
Press,
Cambridge,
Mass.,
1947.
2
Niven,
J.
S.
F.,
"The
Action
of
a
Cytotoxic
Antiserum
on
Tissue
Cultures,"
J.
Path.
and
Bact.,
32,
527
(1929).
3
Lambert,
R.
A.,
and
Hanes,
F.
M.,
"The
Cultivation
of
Tissues
in
vitro
as
a
Method
for
the
Study
of
Cytotoxins,"
J.
Exper.
Med.,
12,
453
(1911).
'Verne,
J.,
and
Oberling,
C.,
"Action
des
Serums
Cytotoxiques
sur
les
Tissus
Cul-
tives
in
vitro,"
Compt.
Rend.
Soc.
Biol.,
109,
860
(1932).
6
Harris,
M.,
"Specificity
and
Mode
of
Action
of
Cytotoxins
Produced
against
Alien
Transplants
in
Rats,"
J.
Exper.
Zool.,
107,
439
(1948).
6
Cameron,
G.,
Tissue
Culture
Technique,
Academic
Press,
Inc.,
New
York,
1950.
7Chambers,
R.,
and
Kempton,
R.
T.,
"Indications
of
Function
of
the
Chick
Meso-
nephros
in
Tissue
Culture
with
Phenol
Red,"
J.
Cell.
and
Comp.
Physiol.,
3,
131
(1933).
8
Masugi,
M.,
Sato,
Y.,
Murasawa,
S.,
and
Tomizuka,
Y.,
"tYber
die
experimentelle
Glomerulonephritis
durch
das
spezifische
Antinierenserum,"
Tr.
Jap.
Path.
Soc.,
22,
614
(1932).
9
Lange,
K.,
Gold,
M.
M.
A.,
Weiner,
D.,
and
Simon,
V.,
"Autoantibodies
in
Human
Glomerulonephritis,"
J.
Clin.
Invest.,
28,
50
(1949).
10
Addis,
T.,
Glomerular
Nephritis,
The
Macmillan
Co.,
New
York,
1948.
THE
EXCITATORY
PROCESS
IN
THE
COCHLEA*
BY
H.
DAVIS,
C.
FERNkNDEZ,f
AND
D.
R.
MCAULIFFE
CENTRAL
INSTITUTE
FOR
THE
DEAF,
ST.
Louis,
MiSSOuRi
Read
before
the
Academy,
April
27,
1949,
and
April
24,
19504
Introduction.-The
nature
of
the
excitatory
process
by
which
sensory
cells
initiate
nerve
impulses
in
afferent
nerve
fibers
is
very
obscure.
In
the
case
of
the
ear,
the
most
widely
accepted
theory
has
been
that
an
electrical
potential
known
as
the
"cochlear
microphonic"
is
generated
by
the
hair
cells
in
the
organ
of
Corti
and
serves as
a
direct
electrical
stimulus
to
the
peripheral
terminations
of
the
fibers
of
the
auditory
nerve.
The
cochlear
microphonic,
it
will
be
recalled,
seems
to
be
simultaneous
with
the
mechanical
movements
of
the
cochlear
partition
and
it
follows
the
wave
form
of
the
sound
very
closely,
at
least
at
moderate
intensities
of
stimulation.
It
shows
no
refractory
period
or
all-or-none
characteristics
like
the
action
potentials
of
nerve.'
Action
potentials
of
the
auditory
nerve,
probably
generated
in
the
cell
bodies
in
the
spiral
ganglion,
not
in
the
fine
non-myelinated
terminal
twigs,
can
also
be
recorded
from
electrodes
placed
in
or
near
the
cochlea.
580
PROC.
N.
A.
S.
PHYSIOLOGY:
DAVIS,
ETAL.
58
Sound
waves
at
2000
to
6000
cycles
per
second
are
very
efficient
as
auditory
stimuli.
This
high
efficiency
led
Weverl
and
one
of
the
present
authors2
to
postulate
an
intermediate
excitatory
effect
or
process
which
had
the
property
of
summating
the
excitatory
effects
of
two
or
more
sound
waves.
We
now
present
experimental
evidence
for
the
existence
of
such
a
process
of
summation.
We
also
have
found
a
third
electrical
potential
in
the
cochlea
in
addition
to
the
cochlear
microphonic
and
nerve
action
potentials.
The
new
potential
exhibits
summation
and
seems
to
represent
the
local
excitatory
process
that
initiates
auditory
nerve
impulses.
Methods.-AII
experiments
were
performed
on
guinea
pigs
anesthetized
with
dial
in
urethane.
Electrodes
consisting
of
No.
38
enamel-insulated
silver
wire
were
introduced
into
the
cochlea
through
small
holes
drilled
into
scala
tympani,
scala
vestibuli
and/or
scala
media3'
4
of
the
basal
turn.
ELECTRODES
IN
FIRST
TURN
OF
GUINEA
PIG'S
COCHLEA
VESTISL
SCALA
~~~~~~~~~Smatlng
SOF
COAT,
+
ouda
BULLA
BRAIN
C@cvMl
ru-DnEC
REFERENCE
ELECTRODE
(ON
NECK~)
FIGURE
1
(In
some
experiments
electrodes
were
placed
in
other
turns
as
well.)
The
position
in
turn
1
is
at
the
site
of
maximal
stimulation
by
tones
of
8000
c.
p.
s.
The
electrical
circuit
was
completed
by
a
reference
electrode
attached
to
the
wound
in
the
neck.
The
cochlea
of
the
guinea
pig
pro-
trudes
into
an
air-filled
bulla,
and
thus
the
electrical
circuit
from
the
reference
electrode
enter;
the
cochlea
chiefly
by
way
of
the
internal
audi-
tory
meatus.
The
reference
electrode
is
thus
roughly
equivalent
to
one
placed
on
the
auditory
nerve.
Electrical
responses
were
recorded
simultaneously
from
several
combi-
nations
of
electrodes
by
means
of
a
three-channel
cathode-ray
oscilloscope
assembly
(Grass).
Two
of
the
channels
could
be
connected
in
parallel
so
as
to
either
add
or
subtract
the
signal
in
one
to
(or
from)
the
signal
in
the
other.3'
4
In
this
way
the
action
potential
of
the
auditory
nerve,
which
appears
as
a
negative
electrical
change
at
all
of
the
cochlear
electrodes,
VOL.
36,
1950
581
PHYSIOLOG
Y:
DA
VIS,
ET
AL.
could
be
completely
canceled
by
subtracting
the
scala
tympani
signal
from
the
scala
vestibuli
signal,
after
appropriate
adjustment
of
amplification.
The
cochlear
microphonic,
on
the
other
hand,
appears
in
opposite
phase
in
scala
tympani
from
what
it
is
in
scala
vestibuli
and
scala
media
(see
Fig.
1).
It
can
be
canceled
by
adding
the
signals
from
scala
vestibuli
(or
media)
and
scala
tympani.
By
this
method
action
potentials
of
moderate
voltage
can
be
viewed,
and
their
latency
measured,
in
spite
of
the
simultaneous
presence
of
a
large
cochlear
microphonic
which
otherwise
usually
obscures
them
almost
completely.
The
acoustic
stimuli
employed
included
clicks
and
pure
tones,
but
were
chiefly
brief
tone-pips.
Our
usual
"tone-pip"
consisted
of
sound
waves
at
a
basic
frequency
of
8000
c.
p.
s.
This
signal
begins
gradually
and
reaches
maxim.m
amplitude
during
the
fourth
or
fifth
wave
and
immediately
diminishes
again
(see
Fig.
3).
The
"2000
c.
p.
s.
tone-pip"
has
a
basic
frequency
of
2000
c.
p.
s.
The
maximum
in
this
case
is
reached
2000
cps
TONE
-
PIPS
640-AA
MICROPHONE
BASAL
TURN
or
GUINEA
PIGS
COCHLEA
VESTISWU
-TYMPM
VESTIBULI
ALONE
VESTAIJ
TTMWS
POLAWrv
Of
ACOUSTIC
STIMULUS
MICROPHONIC
NO
CANCELLATION
ACTION
POTENTIAL
STIALB
PIPS
ARtE
40
DO
ABOVE
THIBESI4OLD
Or
ACTION
POTENTIALS
ACT1B
POBTtiALS
ANS
SAMMPB
D
00A
A
SIALAL
ASorT
OF
UWAPABLLIE
CD
SICSIONIC
AND
VJUTn
G
POTMA^L
l
R-PS111
TO
TWO
PSf
Or
ORRSITt
POL.ASATi
SHW
A
wrvSMtSWA
IN
LATtNcy
or
ACTION
PoTBOTA
L&
+
OOOSLC
SPOSAOS
POCITOAAPS
SEOCTHD
*
1
FIGURE
2
during
the
third
sound
wave.
The
pips
were
presented
at
pulsing
fre-
quencies
from
1
to
60
per
second.
The
tone-pips
have
several
advantages:
(1)
nearly
all
of
the
acoustic
energy
is
concentrated
in
a
band
less
than
an
octave
wide6
so
that
they
presumably
activate
a
relatively
restricted
region
of
the
cochlear
partition,
yet
(2)
the
relatively
rapid
onset
may
allow
identification
of
the
particular
sound
wave
that
initiates
a
nerve
impulse
and
(3)
at
frequencies
of
1000
c.
p.
s.
and
higher
only
one
impulse
is
set
up
in
each
fiber
because
of
the
rapid
increment
and
decrement
of
sound
waves
and
the
refractory
period
of
the
nerve
fibers.
Evidence
for
Summation.-For
frequencies
of
2000
c.
p.
s.
and
less,
each
volley
of
nerve
impulses
revealed
by
the
action
potential
can
be
clearly
associated
with
one
sound
wave
or
another.
We
find
that
only
the
portion
PRtOC.
N.
A.
S.
582
PHYSIOLOGY:
DA
VIS,
ET
AL.
of
the
wave
corresponding
to
acoustic
rarefaction
at
the
ear
drum
causes
auditory
stimulation.
If
one
(negative)
wave
in
a
tone-pip
has
set
up
an
action
potential,
the
next
wave,
if
stronger,
may
activate
other
neurons
of
higher
threshold
even
though
the
neurons
stimulated
by
the
first
wave
are
still
refractory.
Thus
the
composite
action
potential
may
show
two
peaks
separated
by
one
wave-length
of
the
basic
frequency
of
the
tone-pip
(see
Fig.
2).
Reversal
of
the
polarity
of
the
tone-pip,
i.e.,
starting
with
a
negative
instead
of
a
positive
sound
wave,
will
change
the
latency
of
the
first
effective
sound
wave
because
the
first
adequate
negative
sound
wave
now
comes
either
a
half
wave
earlier
or
a
half
wave
later
than
it
did
pre-
viously.
(The
first
effective
wave
may
be
either
stronger
or
weaker
than
the
first
effective
wave
with
the
original
polarity.
The
two
peaks
of
action
potentials
will
in
general,
therefore,
be
different
in
amplitude
as
well
as
showing
a
difference
in
latency.
Both
of
these
effects
are
illustrated
in
figure
2.)
The
basic
frequency
employed
in
figure
2
was
2000
c.
p.
s.
and
it
is
clear
that
at
this
frequency
the
auditory
nerve
is
responding
to
individual
sound
waves
in
the
tone-pip.
8000
cps
TONE-PIPS
640-AA
LACROPHONE
BASAL
TURN
OF
GUINEA
PIG'S
COCHLEA
SCALA
VESTIWLI
VESTISLI
AND
TYMD
M
ACOUSTIC
STIMULUS
NO
CANCELLATION
MIX
-
MCROPHONIC
Mx
ACTION
O
AD
POTENTIAL
"wsL
j
f
22
fMW
.
RCPETo
-TWV
-E
I
TwuOM.S.
TO
T
,nWAL,
or
f
I\
AThfX
.T
Iv
/11
3
COOStNT
LAV
v
.
at
,.
P4
/AI
NW
SIGEK,
SUMMATING
POTENTIAL
FIGURE
3
With
a
basic
frequency
of
8000
c.
p.
s.,
however,
the
behavior
of
the
nerve
is
fundamentally
different.
There
is
no
visible
change
in
latency
when
the
polarity
of
the
tone-pip
is
reversed
(see
Fig.
3).
We
have
sought
for
a
change
of
latency
with
great
care
on
the
face
of
the
oscilloscope
and
have
assured
ourselves
that
if
there
is
a
change
of
latency
it
is
certainly
less
than
30
microseconds.
The
change
which
should
occur
if
the
nerve
were
re-
sponding
to
individual
sound
waves
is
62
microseconds.
We
conclude
that
at
this
frequency
the
nerve
does
not
respond
to
individual
sound
waves
but
that
a
stimulating
effect
is
carried
over,
even
from
the
earliest
sub-
liminal
waves.
The
stimulating
effects
are
integrated
by
some
process
that
we
call
"summation"
so
that
the
nerve
responds
to
the
tone-pip
as
a
whole
instead
of
to
the
individual
waves.
Summation
seems
to
dominate
the
picture
at
8000
c.
p.
s.
(At
4000
c.
p.
s.
a
small
change
of
latency
with
reversal
of
polarity
can
still
be
demonstrated,
however.)
VOL.
36,
1950
583
PH
YSIOLOG
Y:
DA
VIS,
ET
AL.
A
second
line
of
evidence
for
summation
at
high
frequencies
is
found
in
the
change
of
latency
with
the
intensity
of
a
tone-pip.
At
low
frequencies
the
latency
diminishes
in
stepwise
fashion
as
the
intensity
of
the
stimulus
is
increased.
Each
step
means
that
an
earlier
sound
wave,
originally
too
weak
to
stimulate,
has
now
become
strong
enough
to
set
up
nerve
impulses.
At
2000
c.
p.
s.
the
number
of
steps
that
can
be
observed
corre-
sponds
to
the
number
of
sound
waves
(counting
only
the
negative
peaks)
from
the
beginning
of
the
tone-pip
to
the
largest
negative
peak.
At
8000
RESPONSES
TO
TONE-PIPS:
BASALTURN
OF
GUINEA
PIGS
COCHLEA
CANCELLATION
SCALA
VESTIBULI
VESTIBULI
+
TYMPANI
DB
ABOVE
ORIGINAL
^
~~~~~~A.P
THRESHOLD
A
2000
CPS
A.P
TRH
34
220:
22
MAY
19
I'
ACTION
POTENTIALS
SCALA
VESTIBULI
SCALA
MEDIA
B
8000
CPS
|
74
223
31
MAY
1950
Mac
8
SUMMATING
POTENTIAL
FIGURE
4
A.
Cancellation
of
cochlear
microphonic
of
2000
c.
p.
s.
tone-pip
(gains
adjusted
to
give
minimum
residue)
reveals
two
volleys
of
action
potentials
(I)
separated
by
one
wave-
length
of
the
stimulating
frequency.
They
are
preceded
by
small
waves
of
summating
potential
and
cochlear
microphonic
in
uncertain
proportion.
The
late
waves
(II)
include
the
second
neural
response
(from
the
cochlear
nucleus
in
the
me-
dulla).
B.
Responses
from
scala
vestibuli
and
from
scala
media
(slightly
retouched).
No
cancellation.
In
this
experiment
the
cochlear
microphonic
disappeared
almost
completely
when
an
electrode
was
inserted
into
scala
media.
Small
action
potentials
are
visible
and
the
8000
c.
p.
s.
ripple
is
partly
cochlear
microphonic
but
the
main
deflections
are
summating
potential.
An
upward
deflection
means
cochlea
more
positive
to
reference
electrode.
c.
p.
s.,
however,
the
shortening
of
latency
as
intensity
increases
seems
to
be
continuous.
More
important,
the
total
shortening
as
the
stimulus
is
increased
from
threshold
to
a
rather
high
level
may
be
greater
by
at
least
two
wave-lengths
than
the
time
from
the
beginning
of
the
pip
to
the
largest
wave.
It
seems,
therefore,
that
at
threshold
the
process
of
stimula-
tion
must
have
been
completed
by
a
wave
later
than,
and
therefore
smaller
than,
the
maximum
wave
at
the
center
of
the
tone-pip.
We
believe
that
this
is
good
supporting
evidence
for
the
existence
of
summation,
although
584
PROC.
N.
A.
S.
PH
YSIOLOG
Y:
DA
VIS,
ETAL.
the
argument
makes
the
tacit
but
unproved
assumptions
that
the
conduc-
tion
time
for
the
nerve
impulse
and
also
the
time
required
for
the
excitatory
process
to
set
off
a
nerve
impulse
are
the
same
whether
the
stimulus
be
weak
or
strong.
The
Summating
Potential.-About
a
year
ago6
we
described
what
we
called
"rectification"
of
the
cochlear
microphonic.
Under
several
adverse
circumstances,
such
as
anoxia,
the
electrocoagulation
of
part
of
the
cochlea,
or
the
insertion
of
several
electrodes
deeply
into
the
cochlea,
the
cochlear
microphonic
may
apparently
shrink
to
a
few
per
cent
of
its
original
ampli-
tude.
The
remaining
response
is
"rectified,"
meaning
that
only
one-half
of
each
wave
(the
half
in
which
scala
vestibuli
becomes
electrically
nega-
tive)
still
remains.
This
description
is
adequate
for
frequencies
below
2000
c.
p.
s.
We
have
recently
observed
that
at
higher
frequencies
there
is
also
a
shift
of
the
base
line
in
the
direction
of
negativity
in
the
scala
vestibuli.
The
negative
deflection
appears
to
be
produced
by
fusion
of
successive
electrical
pulses
that
recur
with
the
frequency
of
sound
waves.
With
an
8000
c.
p.
s.
tone-pip
the
pattern
resembles
the
negative
half
of
the
envelope
of
the
pip,
with
an
8000
c.
p.
s.
ripple
also
clearly
visible
(see
Fig.
4).
These
"rectified"
potentials
are
actually
quite
independent
of
the
cochlear
microphonic.
They
represent
a
third
electrical
potential
of
the
cochlea
which shows
the
property
of
summation
at
frequencies
above
2000
c.
p.
s.
This
third
potential
decays
rapidly
enough,
however,
so
that
there
is
usually
no
effective
carry-over
(summation)
below
2000
c.
p.
s.
The
maximum
voltage
of
the
third
potential
has
not
yet
been
measured
because
of
serious
technical
limitations
but
it
is
well
over
50
microvolts
(scala
media
vs.
reference
electrode).
Evidence
that
the
summating
potential
differs
from
both
the
cochlear
microphonic
and
the
action
potential
is
as
follows:
1.
The
summating
potential
(SP)
is
unidirectional
(like
the
action
po-
tential)
for
any
particular
pair
of
electrodes.
The
cochlear
microphonic
(CM),
on
the
other
hand,
is
a
change
of
electrical
potential
both
above
and
below
the
original
resting
level.
2.
SP
shows
summation.
It
outlasts
the
mechanical
movement
(unlike
CM)
and
it
shows
no
all-or-none
behavior
or
refractory
period
(unlike
action
potentials
(AP)).
3.
SP
and
CM
are
differently
oriented
anatomically.
The
most
favorable
combination
of
electrodes
for
recording
SP
is
scala
media
vs
reference
electrode.
The
most
favorable
combination
for
CM
is
scala
vestibuli
vs.
scala
tympani.
Figure
1
shows
how
these
axes
are
approxi-
mately
at
right
angles
to
one
another.
4.
The
anatomical
location
of
SP
is
apparently
in
the
organ
of
Corti
(like
CM)
and
not
in
the
spiral
ganglion
(uinlike
AP).
AP
appears
equally
and
in
the
same
direction
at
electrodes
in scala
vestibuli,
media
or
tympani
VOL.
36,
1950
585
PHYSIOLOGY:
DAVIS,
ETAL.
(vs.
reference
electrode).
SP
appears
strongly
in scala
media
(vs.
refer-
ence)
but
may
be
completely
absent
in
scala
tympani
(unlike
CM
and
AP),
or,
if
the
electrode
is
placed
as
far
as
possible
away
from
the
basilar
membrance,
its
sign
may
actually
be
reversed.
The
possibility
of
placing
an
electrode
on
the
positive
side
of
the
isopotential
line
in
scala
tympani
shows
that
the
origin
of
the
potential
difference
must
be
well
out
in
the
cochlear
canal
and
not
within
the
modiolus.
5.
The
SP
lags
in
time
(or
phase)
behind
CM.
If
CM
from
scala
tympani
is
used
to
cancel
CM
from
scala
vestibuli,
some
SP
as
well
as
AP
therefore
remains
(see
Fig.
4
A).
The
lag
seems
to
be
of
the
order
of
100
microseconds.
6.
The
SP
may
remain
in
the
face
of
adverse
conditions,
such
as
anoxia
or
operative
trauma,
after
the
cochlear
microphonic
has
virtually
or
com-
pletely
disappeared.
Action
potentials
have
been
observed
under
such
conditions
of
operative
trauma.
This
point
is
of
special
importance
as
it
shows
that
neither
the
summating
potential
nor
the
action
potentials
are
in
any
way
dependent
on
the
cochlear
microphonic.
The
cochlear
microphonic
may
be
a
good
indicator
of
the
time
and
a
fair
indicator
of
the
intensity
of
mechanical
movement
of
the
organ
of
Corti,
but
it
is
not
part
of
the
chain
of
events
that
generates
the
nerve
impulse.
7.
At
high
intensities
of
stimulation,
although
still
within
limits
per-
fectly
tolerable
to
the
human
ear,
the
SP
continues
to
increase
with
the
intensity
of
the
8000
c.
p.
s.
tone-pips,
although
the
increase
(like
that
of
CM)
becomes
non-linear.
While
SP
is
still
increasing
CM
reaches
its
maximum
and
may
even
begin
to
shrink
again.
It
is
worth
noting
that
the
behavior
of
SP
is
more
in
line
with
the'behavior
of
AP,
which
is
still
increasing
at
this
intensity,
not
to
mention
the
sense
of
loudness to
the
human
ear
which
is
also
still
increasing.
8.
Electrical
polarization
between
scala
vestibuli
and
scala
tympani
increases
or
decreases
SP
according
to
its
direction.
When
the
SP
is
increased
the
AP
increases
also.
When
SP
is
diminished
AP
diminishes
or
vanishes.
The
same
intensity
of
electrical
polarization
causes
a
small,
but
only
very
small,
change
in
the
cochlear
microphonic.
If
the
cochlear
microphonic
is
already
absent
it
may
be
restored
(or
an
equivalent
micro-
phonic
may
be
introduced)
by
electrical
polarization.
The
polarity
of
the
microphonic
relative
to
the
sound
wave
will
in
this
case
depend
on
the
direction
of
the
polarizing
current.
We
have
not
been
able
to
reverse
SP
by
polarization.
9.
On
the
death
of
the
animal
AP
disappears
first;
SP
continues
for
a
time
after
death;
CM
may
continue
longer,
although
at
the
low
post-
mortem
level
that
is
already
so
familiar.7
Sometimes
SP
outlasts
CM.
Interpretation
of
the
Summating
Potential.-We
believe
that
the
sum-
mating
potential
arises
in
the
terminal
twigs
of
the
auditory
nerve
fibers
586
PROC.
N.
A.
S.
PH
YSIOLOG
Y:
DA
VIS,
ET
AL.
which
are
arranged
like
baskets
around
the
hairless
ends
of
the
hair
cells.
We
believe
also
that
the
summating
potential
is
a
local
excitatory
process
analogous
to
the
end-plate
potential
at
the
neuro-myal
junction
and
to
the
post-synaptic
potentials
of
spinal
neurons.8
How
the
mechanical
move-
ment
sets
up
the
local
excitatory
process
(the
summating
potential)
is
unknown.
The
latency
of
the
action
potential
relative
to
the
mechanical
move-
ment
we
interpret
as
due
mostly
to
conduction
time
from
the
nerve
endings
to
the
cell
bodies.
The
shortest
latency
that
we
have
measured
for
the
foot
of
the
action
potential
from
the
beginning
of
the
cochlear
microphonic
following
a
strong,
sharp
click
(rarefaction)
is
550
microseconds.
General
Significance.-We
have
described
a
summating
potential
which
seems
to
represent
the
excitatory
process
initiated
by
the
sensory
cells
of
the
cochlea
in
their
afferent
nerve
fibers.
Similar
electrical
potentials,
probably
representing
the
same
type
of
excitatory
process,
have
been
re-
corded
from
muscle
spindles9
and
from
Pacinian
corpuscles,'0
and
by
analogy
we
may
expect
to
find
them
also
in
the
related
sense
organs
for
touch,
pressure,
vibration,
muscle
sense,
orientation
to
gravity
and
acceler-
ation.
The
summating
potential
in
the
ear
and
perhaps
elsewhere
should
be
a
useful
tool
for
determining
the
mode
of
action
of
drugs,
fatigue,
etc.,
on
the
sense
organ
and
for
investigation
of
the
process
whereby
mechanical
force
initiates
the
excitatory
process.
*
This
work
was
carried
out
under
Contract
N6onr-272
between
the
Office
of
Naval
Research
and
Central
Institute
for
the
Deaf.
t
Former
Fellow
of
the
W.
K.
Kellogg
Foundation.
t
Read
under
the
titles:
"Audition-A
Physiological
Survey"
and
"Summation
in
the
Auditory
Sensory
Process."
Some
material
has
been
added
in
preparing
the
paper
for
the
press.
1
Wever,
E.
G.,
Theory
of
Hearing,
John
Wiley
&
Sons,
Inc.,
New
York,
1949,
484
pp.
2
Davis,
H.,
unpublished,
but
reported
at
the
meeting
of
the
National
Academy
of
Sciences,
April
24,
1949.
3
Davis,
H.,
Gernandt,
B.
E.,
Riesco-MacClure,
J.
S.,
and
Covell,
W.
P.,
J.
Acoust.
Soc.
Am.,
21,
502-510
(1949).
4
Davis,
H.,
Gernandt,
B.
E.,
and
Riesco-MacClure,
J.
S.,
J.
Neurophysiol.,
13,
73-87
(1950).
6
Davis,
H.,
Silverman,
S.
R.,
and
McAuliffe,
D.
R.,
"A
Test
of
the
Frequency
Theory
of
Hearing"
(in
preparation
for
J.
Acoust.
Soc.
Am.)
6
Riesco-MacClure,
J.
S.,
Davis,
H.,
Gernandt,
B.
E.,
and
Covell,
W.
P.,
Proc.
Soc.
Exptl.
Biol.
and
Med.,
71,
158-160
(1949).
7
Wever,
E.
G.,
Bray,
C.
W.,
and
Lawrence,
M.,
Ann.
Otol.
Rhinol.
Laryngol.,
50,
317-329
(1941).
8
Brooks,
C.
McC.,
and
Eccles,
J.
C.,
Nature,
159,
760-764
(1947).
9
Katz,
B.,
"The
Electric
Response
at
a
Sensory
Nerve
Ending,"
J.
Physiol.,
109,
9P-1OP
(1949).
10
Scott,
D.,
Jr.,
"The
Response
Pattern
of
the
Pacinian
Corpuscle,"
Am.
J.
Med.
Sci.,
217,
355
(1949).
VtOL.
36,
1950
587
... For phase inversions, three explanations have been proposed in the literature. First, CM recordings from the scala vestibuli have a polarity opposite that for scala tympani recordings (Davis et al., 1950) caused by the hair cells acting as an electrical dipole (Hudspeth, 1982). Phase inversions could therefore indicate scalar dislocations. ...
... This amplitude decrease may have caused the ANN to dominate the recordings, leading to harmonic distortions. Although phase inversions due to dipole behavior have previously been suggested to reflect a change in measurement location to a different scala (Davis et al., 1950), which does not seem to be the case in our data, the complex electrical properties of the cochlea make the spread of the electric field resulting from the hair cell dipole difficult to predict (Hudspeth, 1982). Our data therefore suggest that dipole behavior may occur even with same-scalar insertions, although further research will be needed to confirm this. ...
Article
Full-text available
The use of electrocochleography (ECochG) for providing real-time feedback of cochlear function during cochlear implantation is receiving increased attention for preventing cochlear trauma and preserving residual hearing. Although various studies investigated the relationship between intra-operative ECochG measurements and surgical outcomes in recent years, the limited interpretability of ECochG response changes leads to conflicting study results and prevents the adoption of this method for clinical use. Specifically, the movement of the recording electrode with respect to the different signal generators in intracochlear recordings makes the interpretation of signal changes with respect to cochlear trauma difficult. Here, we demonstrate that comparison of ECochG signals recorded simultaneously from intracochlear locations and from a fixed extracochlear location can potentially allow a differentiation between traumatic and atraumatic signal changes in intracochlear recordings. We measured ECochG responses to 500 Hz tone bursts with alternating starting phases during cochlear implant insertions in six human cochlear implant recipients. Our results show that an amplitude decrease with associated near 180° phase shift and harmonic distortions in the intracochlear difference curve during the first half of insertion was not accompanied by a decrease in the extracochlear difference curve’s amplitude ( n = 1), while late amplitude decreases in intracochlear difference curves (near full insertion, n = 2) did correspond to extracochlear amplitude decreases. These findings suggest a role for phase shifts, harmonic distortions, and recording location in interpreting intracochlear ECochG responses.
... Initial studies of the SP suggested a possible neural origin (Davis et al. 1950;Kupperman, 1966), but over time, these were discounted for a purely hair cell origin based on asymmetries in the CM primarily of OHCs (Dallos et al. 1972;Dallos 1973;Dallos and Cheatham 1976). However, asymmetries are greater in IHCs than OHCs (see Fig. 6) and have opposite polarities, at least as recorded at the round window. ...
Article
Using electrocochleography, the summating potential (SP) is a deflection from baseline to tones and an early rise in the response to clicks. Here, we use normal hearing gerbils and gerbils with outer hair cells removed with a combination of furosemide and kanamycin to investigate cellular origins of the SP. Round window electrocochleography to tones and clicks was performed before and after application of tetrodotoxin to prevent action potentials, and then again after kainic acid to prevent generation of an EPSP. With appropriate subtractions of the response curves from the different conditions, the contributions to the SP from outer hair cells, inner hair cell, and neural "spiking" and "dendritic" responses were isolated. Like hair cells, the spiking and dendritic components had opposite polarities to tones - the dendritic component had negative polarity and the spiking component had positive polarity. The magnitude of the spiking component was larger than the dendritic across frequencies and intensities. The onset to tones and to clicks followed a similar sequence; the outer hair cells responded first, then inner hair cells, then the dendritic component, and then the compound action potential of the spiking response. These results show the sources of the SP include at least the four components studied, and that these have a mixture of polarities and magnitudes that vary across frequency and intensity. Thus, multiple possible interactions must be considered when interpreting the SP for clinical uses.
... The CM baseline shift following the envelope of the CM was named the summating potential (SP) (Davis et al., 1950Smith et al., 1958;Cheatham and Dallos, 1984;Dallos, 1975;Dallos et al., 1970). The polarity of SP is defined as the polarity of the potential change on the vestibular side of the organ of Corti (scala vestibuli or scala media) relative to scala tympani or to a distant reference electrode. ...
Chapter
Synopsis This chapter describes the sensory organ and processes by which hearing occurs. Sound travels through the external ear canal and the middle ear to the cochlea, a snail like structure in the temporal bone, and vibrates the delicate soft tissue structures of the cochlea. The acoustic signals are then separated into small frequency bands, each of which vibrates a particular portion of the cochlea and creates a frequency-place representation. Specialized cells, the hair cells, sense and transform the vibration into a sequence of electrical pulses, which travel along the auditory nerve to the brain and ultimately result in an auditory percept, such as speech or music.
... Typically, it is described as a hair cell potential produced by asymmetries in cochlear transduction to the two directions of stereociliary movement (Whitfield and Ross 1965). A neural contribution is rarely considered in descriptions of the SP (Eggermont 2017;Hornibrook 2017;Russell 2008), although it has been suggested in the past (Davis et al. 1950;Kupperman 1966), and animal experiments using neurotoxins have shown a reduction in the SP magnitude Sellick et al. 2003;van Emst et al. 1995). To better understand the underlying processes, we report in this article the results of pharmacological experiments in gerbils that are intended to isolate the individual contributions of outer hair cells (OHCs), inner hair cells (IHCs), and neural sources to the SP. ...
... Our algorithm indicates that phase changes not near the complete inversion range of 180 degrees are associated with translocation perhaps indicating a random dissociation between the leading and training signals. This contention is supported by previous animal work (29,30). While these initial results are promising for clinical applicability, understanding the nuances of patient specific ECochG recordings will require many additional data sets. ...
Article
Hypothesis: Electrocochleography (ECochG) patterns observed during cochlear implant (CI) electrode insertion may provide information about scalar location of the electrode array. Background: Conventional CI surgery is performed without actively monitoring auditory function and potential damage to intracochlear structures. The central hypothesis of this study was that ECochG obtained directly through the CI may be used to estimate intracochlear electrode position and, ultimately, residual hearing preservation. Methods: Intracochlear ECochG was performed on 32 patients across 3 different implant centers. During electrode insertion, a 50-ms tone burst stimulus (500 Hz) was delivered at 110 dB SPL. The ECochG response was monitored from the apical-most electrode. The amplitude and phase changes of the first harmonic were imported into an algorithm in an attempt to predict the intracochlear electrode location (scala tympani [ST], translocation from ST to scala vestibuli [SV], or interaction with basilar membrane). Anatomic electrode position was verified using postoperative computed tomography (CT) with image processing. Results: CT analysis confirmed 25 electrodes with ST position and 7 electrode arrays translocating from ST into SV. The ECochG algorithm correctly estimated electrode position in 26 (82%) of 32 subjects while 6 (18%) electrodes were wrongly identified as translocated (sensitivity = 100%, specificity = 77%, positive predictive value = 54%, and a negative predictive value = 100%). Greater hearing loss was observed postoperatively in participants with translocated electrode arrays (36 ± 15 dB) when compared with isolated ST insertions (28 ± 20 dB HL). This result, however, was not significant (p = 0.789). Conclusion: Intracochlear ECochG may provide information about CI electrode location and hearing preservation.
... Despite its first description in the 1950s (Davis et al., 1950(Davis et al., , 1958, the origin of the SP is still a matter of considerable debate in terms of contributions from inner and outer hair cells and neural sources. Early work suggested outer hair cell sources predominate (Dallos and Cheatham, 1976) but later studies that removed inner hair cells in chinchillas showed a large effect on the CM (Zheng et al., 1997;Durrant et al., 1998). ...
Article
Full-text available
Auditory neuropathy spectrum disorder (ANSD) is characterized by an apparent discrepancy between measures of cochlear and neural function based on auditory brainstem response (ABR) testing. Clinical indicators of ANSD are a present cochlear microphonic (CM) with small or absent wave V. Many identified ANSD patients have speech impairment severe enough that cochlear implantation (CI) is indicated. To better understand the cochleae identified with ANSD that lead to a CI, we performed intraoperative round window electrocochleography (ECochG) to tone bursts in children (n = 167) and adults (n = 163). Magnitudes of the responses to tones of different frequencies were summed to measure the “total response” (ECochG-TR), a metric often dominated by hair cell activity, and auditory nerve activity was estimated visually from the compound action potential (CAP) and auditory nerve neurophonic (ANN) as a ranked “Nerve Score”. Subjects identified as ANSD (45 ears in children, 3 in adults) had higher values of ECochG-TR than adult and pediatric subjects also receiving CIs not identified as ANSD. However, nerve scores of the ANSD group were similar to the other cohorts, although dominated by the ANN to low frequencies more than in the non-ANSD groups. To high frequencies, the common morphology of ANSD cases was a large CM and summating potential, and small or absent CAP. Common morphologies in other groups were either only a CM, or a combination of CM and CAP. These results indicate that responses to high frequencies, derived primarily from hair cells, are the main source of the CM used to evaluate ANSD in the clinical setting. However, the clinical tests do not capture the wide range of neural activity seen to low frequency sounds.
Chapter
This chapter discusses the anatomy and physiology of the inner ear, with emphasis on the vestibular organs and functions, and the vestibular pathways in the central nervous system. An operational model of the vestibular system is included, exploring the mechanisms that are particularly relevant to its clinical evaluation. It must be taken into consideration that the new neurotology is essentially derived from the advances in neurophysiological knowledge.
Article
“Tone‐pips” with a basic frequency of 2000 c.p.s. were produced by passing rectangular pulses of duration through two sound‐effects filter sections in cascade. The high pass and the low pass cut‐offs (18 db per octave) of each unit were set to 2000 c.p.s. The transducer was an Atlas PM 25 loudspeaker. The tone‐pips appear on the oscilloscope as brief trains of waves that begin gradually and reach maximum amplitude at the third wave. The amplitude then falls off only a little less rapidly. A single pip sounds like a metallic click. When the pulses were repeated at 123 per second at sensation levels from 5 to 40 db all of our subjects reported hearing a “buzz.” Other descriptive terms used were “metallic,” “high pitched,” “continuously interrupted,” and “rough.” No listener, even when directly questioned and even when a pure tone of 123 per second had been sounded a few seconds previously for comparison, ever reported any trace of a low pitched component corresponding to 123 per second. Inasmuch as the frequency of nerve impulses in each nerve fiber is 123 per second under these conditions, the absence of a sensation of low pitch is contrary to the frequency theory of pitch perception and favors the place theory even for very low tones.
unpublished, but reported at the meeting of the National Academy of Sciences
  • H Davis
Davis, H., unpublished, but reported at the meeting of the National Academy of Sciences, April 24, 1949.
  • E G Wever
  • C W Bray
Wever, E. G., Bray, C. W., and Lawrence, M., Ann. Otol. Rhinol. Laryngol., 50, 317-329 (1941).
  • H Davis
  • B E Gernandt
  • J S Riesco-Macclure
  • W P Covell
Davis, H., Gernandt, B. E., Riesco-MacClure, J. S., and Covell, W. P., J. Acoust. Soc. Am., 21, 502-510 (1949).
  • J S Riesco-Macclure
  • H Davis
  • B E Gernandt
  • W P Covell
Riesco-MacClure, J. S., Davis, H., Gernandt, B. E., and Covell, W. P., Proc. Soc. Exptl. Biol. and Med., 71, 158-160 (1949).