Effects of Ear Plugging on Single-Unit Azimuth Primary Auditory

JOURNALOF
Vol. 71, No.
NEUROPHYSIOLOGY
6, June 1994. Printed
in U.S.A.
Effects of Ear Plugging on Single-Unit Azimuth Sensitivity in Cat
Primary Auditory Cortex. II. Azimuth Tuning Dependent Upon
Binaural Stimulation
FRANK K. SAMSON, PASCAL BARONE, JANINE C. CLAREY, AND THOMAS J. IMIG
Department of Physiology, Kansas University Medical Center, Kansas City, Kansas 66160- 7401
provided
inhibitory
AND
CONCLUSIONS
SUMMARY
1. Single-unit recordings were carried out in primary auditory
cortex (AI) of barbiturate-anesthetized cats. Observations were
based on a sample of 13 1 high-best-frequency (~5 kHz), azimuthsensitive neurons. These were identified by their responses to a set
of noise bursts, presented in the free field, that varied in azimuth
and sound-pressure level (SPL). Each azimuth-sensitive neuron
responded well to some levels at certain azimuths, but did not
respond well to any level at other azimuths.
2. Unilateral ear plugging was used to infer each neuron’s response to monaural stimulation. Ear plugs, produced by injecting
a plastic ear mold compound into the external ear, attenuated
sound reaching the tympanic membrane by 25-70 dB. The azimuth tuning of a large proportion of the sample (62/ 13 1)) referred to as binaural directional (BD), was completely dependent
upon binaural stimulation because with one ear plugged, these
cells were insensitive to azimuth (either responded well at all azimuths or failed to respond at any azimuth) or in a few cases exhibited striking changes in location of azimuth function peaks. This
report describes patterns of monaural responses and binaural interactions exhibited by BD neurons and relates them to each cell’s
azimuth and level tuning. The response of BD cells to ear plugging
is consistent with the hypothesis that they derive azimuth tuning
from interaural level differences present in noise bursts. Another
component of the sample consisted of monaural directional (27 /
13 1) cells that derived azimuth tuning in part or entirely from
monaural spectral cues. Cells in the remaining portion of the sample (42/ 131) responded too unreliably to permit specific conclusions.
3. Binaural interactions were inferred by statistical comparison
of a cell’s responses to monaural (unilateral plug) and binaural
(no plug) stimulation. A larger binaural response than either
monaural response was taken as evidence for binaural facilitation.
A smaller binaural than monaural response was taken as evidence
for binaural inhibition. Binaural facilitation was exhibited by 65%
( 40/ 62) of the BD sample ( facilitatory cells). Many of these exhibited mixed interactions, i.e., binaural facilitation occurred in response to some azimuth-level combinations, and binaural inhibition to others. Binaural inhibition in the absence of binaural facilitation occurred in 35% (22/62) of the BD sample, a majority of
which were EI cells, so called because they received excitatory (E)
input from one ear (excitatory ear) and inhibitory (I) input from
the other (inhibitory ear). One cell that exhibited binaural inhibition received excitatory input from each ear.
4. EI cells responded vigorously throughout much or all of one
frontal quadrant (preferred side) and responded poorly throughout the other. Plugging of the ear on the nonpreferred side caused
an increase in the cell’s responsiveness, showing that the ear on the
preferred side provided excitatory input and that the other ear
2194
0022-3077/94
$3.00 Copyright
input. For a majority ( 86%, 18/2 1), the preferred side was located contralateral to the recording site in AI.
5. The binaural facilitation group was composed of midlinepreferring (23%, 9/40) and lateral field (LF) cells (77%, 3 l/40)
that responded selectively to midline and lateral locations, respectively. The LF sample included slightly more ipsilateral-than contralateral-preferring cells (55% vs. 45% and 17/ 3 1 vs. 14/ 3 1).
6. Patterns of monaural excitation varied among cells in the
binaural facilitation group. All midline cells and a few LF cells
failed to respond or responded very weakly to monaural stimulation of either ear. Many LF cells were excited exclusively or predominantly by the ear on the preferred side. Plugging of the non(or less) excitatory ear caused an increase in responsiveness on the
nonpreferred side and a decrease in responsiveness on the preferred side showing that the binaural response was a result of
mixed interactions.
7. Monaural and binaural thresholds to noise stimulation were
obtained at preferred azimuths (locations where binaural azimuth
function values were 275%). Most ( 18/ 19) EI cells exhibited
monaural and binaural thresholds that differed by less than 5 dB,
as was the case for 39% ( 11/28) of the LF sample. The remaining
LF cells and all midline cells exhibited higher monaural than binaural thresholds.
8. A level function for binaural noise stimulation was obtained
at the azimuth where maximum response occurred. As level increased from 0 to 80 dB SPL, response magnitude (spikes/stimulus) commonly increased to a maximum and then decreased, i.e.,
it was a nonmonotonic function of level. Nonmonotonic strength,
defined as the reduction in response magnitude at the highest SPL
tested (80 dB unless the cell ceased to respond at lower levels),
ranged from 0 to 100%. For descriptive purposes, level functions
with nonmonotonic strengths of >50% were classified as NM-type
functions ( 37 /62,60%, of the BD sample), and the remainder as
M-type functions. Under binaural conditions, EI cells more commonly exhibited NM-type ( 8 l%, 17/2 1) than M-type level functions whereas equal numbers of facilitatory cells exhibited M- and
NM-type level functions.
9. Nonmonotonic level tuning exhibited by different cells to
binaural noise stimulation could result from nonmonotonic level
tuning from the excitatory ear, binaural inhibition, or Ievel-dependent binaural facilitation. Monotonic level tuning could result
from monotonic level tuning from the excitatory ear or binaural
facilitation over a broad range of levels. Monaural stimulation of
the excitatory ear can account for the level tuning of many EI cells,
as their responses at preferred azimuths were unaffected by plugging the inhibitory ear. Most facilitatory cells exhibited binaural
and monaural level functions that had different thresholds and/ or
form (monotonic or nonmonotonic) showing that binaural mechanisms strongly contributed to level tuning.
0 1994 The American
Physiological
Society
BINAURAL
DIRECTIONAL
CELLS
IN AI
2195
put from one ear, exhibit a mixture of binaural facilitation
and inhibition, and are similar to EI cells in their preference
for ILDs favoring the excitatory ear (Benson and Teas
1976; Brugge et al. 1969; Kelly and Sally 1988; Phillips and
Irvine 198 1; Reale and Kettner 1986; Semple and Kitzes
1993a,b). Some cells, referred to as TWINS (two-way intensity networks), exhibit facilitation or mixed interactions
and are selective for a specific combination of tonal SPLs
presented to each ear (Semple and Kitzes 1993b).
The results of dichotic studies support a widely accepted
binaural
disparity hypothesis that interrelates azimuth tunINTRODUCTION
ing, ILD tuning, monaural inputs, and binaural interacAuditory cortex (AI) plays an important role in sound tions. PB cells should be selective for midline sound
localization. Cats, dogs, ferrets, monkeys, and humans can sources, EI cells and those exhibiting mixed interactions
respond to sounds after destruction of auditory cortex, should be selective for sound sources on the side of the
showing that they are not deaf, but their accuracy of local- excitatory ear, and TWINS should be selective to narrow
ization in the horizontal plane (azimuth) is impaired se- ranges of level and azimuth. A goal of this study was to
verely (Heffner and Master-ton 1975; Jenkins and Master- determine whether the responses of AI neurons to noise
ton 1982; Jenkins and Merzenich 1984; Kavanagh and stimulation were consistent with this hypothesis. The monaural inputs and binaural interactions of azimuth-sensitive
Kelly 1987; Klingon and Bontecou 1966; Sanchez-Longo
and Forster 1958 ) . Single-unit studies using loudspeakers neurons were characterized by studying the effect of ear
to present sounds in the free field have demonstrated that plugging on unit responses, a simple technique exploited by
many neurons in the high-frequency representation of AI Middlebrooks ( 1987 ) in his study of the cat’s superior collicare azimuth sensitive, meaning that they respond vigor- ulus. Unilateral ear plugging attenuates sound reaching the
ously at some directions but not others (cat: Barrett 197 1; tympanic membrane and thus allows testing a cell’s response to simulated monaural stimulation. Binaural interEisenman 1974; Evans 1968; Imig et al. 1990; Middlebrooks and Pettigrew 198 1; Rajan et al. 1990; Sovijarvi and actions may be inferred by comparing responses to monHyvarinen 1974; monkey: Benson et al. 198 1). Such neu- aural and binaural stimulation.
The results of the study revealed two classesof azimuthrons are presumably important for the representation of
sensitive cells, referred to as binaural directional (BD) and
sound source azimuth in the auditory system. Although
these studies demonstrate the existence of azimuth-sensimonaural directional (MD). BD cells, described in this retive neurons in AI, they reveal nothing about the mecha- port, are insensitive to the azimuth of monaurally presented noise bursts, and their azimuth tuning is completely
nisms that underlie directional tuning.
Many AI neurons in cats and other mammals are sensi- dependent upon binaural stimulation. Their azimuth tuntive to interaural time and level differences present in tone ing and patterns of monaural inputs and binaural interacbursts (reviewed by Clarey et al. 1992; cat: Brugge et al. tions are largely consistent with the binaural disparity hy1964, 1969; Hall and Goldstein 1968; Kitzes et al. 1980; pothesis. In contrast, the azimuth tuning of MD cells is
Phillips and Irvine 198 1, 1983; Reale and Brugge 1990; derived in part or entirely from monaural directional cues,
Reale and Kettner 1986; Semple and Kitzes 1993ab; mon- not from ILD sensitivity ( Samson et al. 1993 ).
key: Brugge and Merzenich 1973; rat: Kelly and Sally 1988;
AI neurons vary in breadth of tuning to noise level. Many
chinchilla: Benson and Teas 1976), and such sensitivity is a neurons with nonmonotonic level functions are selective
for limited ranges of level, and most of these are azimuth
fundamental mechanism of azimuth tuning. High-frequency AI neurons, which are sensitive to interaural level sensitive (Imig et al. 1990). Other azimuth-sensitive neudifferences (ILDs) present in tone bursts, exhibit several rons are more broadly tuned to level, including those with
characteristic patterns of monaural inputs and binaural in- monotonic level functions. Ear plugging revealed several
teractions. EI neurons, so called because they receive excit- distinctive patterns of monaural input and binaural interatory (E) input from one ear and inhibitory (I) input from actions that were associated with monotonic and nonmonthe other, exhibit binaural inhibition, i.e., their response otonic functions. A preliminary report has been presented
decreases when sound-pressure level (SPL) at the inhibielsewhere (Samson and Imig 1990). This work represents a
tory ear exceeds that at the excitatory ear (Brugge and Mer- part of the PhD research conducted by Frank Samson.
zenith 1973; Brugge et al. 1969; Kelly and Sally 1988; Phillips and Irvine 198 1) . Other ILD-sensitive cells exhibit bin- METHODS
aural facilitation, i.e., their binaural response is larger than
Single-unit recordings were obtained from 36 healthy adult cats
their monaural response from either ear (Benson and Teas
with clean external ears and normal thresholds, estimated from
1976; Hall and Goldstein 1968; Kitzes et al. 1980; Phillips
auditory brain stem responses or cortical unit responses. The samand Irvine 198 1; Reale and Kettner 1986). Binaural facilitaple of BD cells that is described in this report was obtained from 25
tion occurs at ILDs near zero in predominantly binaural
cats. Anesthesia was induced with sodium pentobarbital(40
mg/
( PB ) cells, so called because they respond to binaural stimu- kg ip), a venous catheter was inserted in the cephalic vein for
lation but not to monaural stimulation (Kitzes et al. 1980; infusion of drugs and fluids, and a tracheal cannula was inserted.
Phillips and Irvine 198 1). Other cells receive excitatory in- A deep level of anesthesia, sufficient to produce miosis and to
10. Some NM-type facilitatory cells, including those with midline and LF azimuth preferences, may receive binaural facilitation
that is a nonmonotonic function of level at each ear. This type of
binaural interaction was described by Semple and Kitzes in AI of
the cat using dichotic tonal stimulation. The monaural responses
and binaural interactions that were revealed by ear plugging, and
the binaural selectivity of NM-type facilitatory cells to limited
ranges of level and azimuth are consistent with this type of binaural mechanism.
2196
F. K. SAMSON,
P. BARONE,
suppress withdrawal, pinna, and eye-blink reflexes, was maintained throughout the duration of the experiment by supplemental intravenous infusions of sodium pentobarbital ( 1/ 10 to
l/ 15 of the initial dose diluted 1: 1 with Ringer solution) as
needed. This translated into a rate between 1.5-4.0 mg.
kg-’ hr-’ that usually decreased throughout the duration of the
experiment. Atropine sulfate (0.1 mg/ kg im) and dexamethasone
(2 mg/kg iv) were given at the beginning of an experiment as
prophylactic measures to minimize respiratory congestion and
brain edema, respectively. Body temperature was maintained at
38°C with a feedback heating pad.
After induction of anesthesia, a midline incision was made in
the scalp, and a craniotomy was performed to allow access to the
middle ectosylvian gyrus in the left hemisphere. A ~4.75 photograph or a scale drawing of the cortical surface was used for recording the locations of electrode penetrations with respect to the cortical vasculature. A Lucite recording chamber and a stainless steel
head-support tube were attached to the cranium with dental
acrylic and anchor screws. The animal was supported in a frame,
its body resting in a sling, and its head rigidly fixed by clamping the
head-support tube to the frame. To approximate the head position
of an alert cat looking straight ahead, the head was positioned with
the horizontal Horsley-Clarke plane tilting forward and down.
The angle between the Horsley-Clarke horizontal plane and the
horizontal plane parallel to the floor was measured in 11 cats
( 18.5” t 3.1 O,mean t SD) by temporarily attaching a U-shaped
plate to the head by means of blunt ear bars and orbit bars. Pinnae
were pulled upright with silk threads glued to their outer surfaces.
Single-unit recordings were carried out with the animal located
in an electrically shielded, quasi-anechoic, sound-isolation
chamber. Single-unit activity was recorded with glass-insulated,
electrolytically sharpened, platinum-plated, tungsten microelectrodes with impedances between 1.O and 3.0 MQ. The bioelectrical
signal was amplified, filtered, and displayed on an oscilloscope
whose sweep was synchronized with the stimulus. It also was fed to
an audiomonitor and to an amplitude-window discriminator that
sent a pulse to the computer each time a single-unit waveform was
detected. Microelectrodes were advanced by the use of a hydraulic
micromanipulator mounted on top of a recording chamber and
controlled from outside the sound chamber. The recording
chamber was sealed hydraulically during the recording session to
minimize pulsation of the brain because of breathing and blood
circulation. Small marking lesions (5 PA X 5 s) were placed during
electrode penetrations to aid in electrode track reconstruction.
Electrode penetrations were oriented tangential to the cortical surface, in a sagittal vertical plane, or normal to the cortical surface.
Tangential and sagittal penetrations were approximately parallel
to isofrequency contours.
Sound stimulation was presented in the free field using an array
of loudspeakers located in the horizontal plane (parallel to the
floor) that included the interaural line. The array was composed of
25 identical loudspeakers, spaced at 7.5 Ointervals along a semicircular arc, and each loudspeaker was located 0.79 m from the interaural midpoint (center of the array). The array could be rotated
about a vertical axis passing through its center allowing presentation of sound from any direction in the horizontal plane. An optical encoder provided the computer with the angular position of
the support frame holding the loudspeaker array. Sound was delivered from one loudspeaker of the array at a time, and loudspeaker
selection for sound delivery was under computer control. Loudspeakers were adjusted to point toward the center of the array.
In searching for single-unit responses, the azimuth and SPL of
noise bursts were varied systematically to increase the chance of
exciting cells that might be selective to narrow ranges of azimuth
and/or level. Noise bursts were presented sequentially from loudl
J. C. CLAREY,
AND
T. J. IMIG
speakers spaced at 30” intervals throughout the hemifield in front
of the interaural line. At each location, an ascending sequence of
levels was presented that ranged from 0 to 80 dB in 20 dB steps
before changing to the next loudspeaker.
Auditory waveform synthesis, acoustic calibration, stimulus
timing and sequencing, data collection, and data analysis were
controlled by a PDP 11/73 computer. Stimulus waveforms were
generated at an output sample rate of 100 kHz using a 16-bit D/A
converter (Boys Town National Research Hospital), low-pass filtered at 40 kHz (Kemo VBF/8, - 180 dB/octave) to prevent
aliasing, attenuated with computer controllable attenuators, and
amplified. Each loudspeaker was calibrated by placing a microphone (B&K type 4 133 l/2 in) at the center of the loudspeaker
array, aiming it at the loudspeaker, and performing a fast Fourier
transform (FFI’) on the impulse response. Tables of maximum
SPL attainable at different frequencies were derived from FFT
data and stored in a computer-disk file for use during experiments.
Calibration values were relatively independent of the rotational
position of the array ( 2 1.5 dB maximum difference). The array
loudspeakers were identical high-frequency drivers (Polydax,
DTW 12X9T25) with fairly flat frequency responses between 1
and 20 kHz (,t5 dB) that rolled off at 20 dB/octave from 20 to 40
kHz and more steeply above 40 kHz because of the antialias filtering, so that at 50 kHz, the output was -67 dB with respect to the
maximum level between 1 and 20 kHz. The frequency response
characteristics of the loudspeakers were similar, and their maximum outputs at each frequency between 2 and 30 kHz varied <4
dB among speakers, and < 10 dB between 1 and 2 kHz. The noise
waveform was generated using a random number generator that
resulted in an electrical signal with a flat spectrum (O-50 kHz) and
uniform amplitude distribution. We refer to this signal as broadband noise, and the actual spectrum of the noise delivered to the
animal was shaped by the loudspeaker and the antialiasing filter.
The maximum attainable SPL for broad-band noise was 93 & 0.5
dB (unweighted measurement). All surfaces of the sound-isolation chamber and animal support frame were covered with 3-inthick acoustical foam (Illbruck) to reduce echoes. Additional details related to the acoustics of the sound system have previously
been reported (Imig et al. 1990).
Fifty-ms-duration noise and tone pips had linear rise-fall ramps
of 5 ms. For each unit, the number of stimulus repetitions at each
azimuth-level combination was constant, and for different units,
this number ranged from 10 to 20. Stimuli were presented at as
high a rate as practicable (2-5 Hz) without causing a substantial
decrease in unit responsiveness.
During a recording session, poststimulus time histograms, dot
rasters, and displays of spike counts plotted as a function of level
and azimuth, or as a function of frequency, were available to the
experimenters. The times of occurrence of action potentials were
stored in computer-disk files with a resolution of 10 ps for later
analysis. Data analysis was performed using a time window to
eliminate the low rate of spontaneous discharge that was present
in the response of a few single units.
Unilateral ear occlusion was effected by injecting a plastic ear
mold compound (All American Mold Lab, Ear Mold Impression
Material) into the pinna and ear canal. It cured to a soft, plastic
consistency that was easy to remove without leaving residues in
the ear canal. Inspection of the plugs after their removal showed
that they typically filled the external cavity of the pinna and external auditory meatus up to the sharp bend located - 13 mm from
the tympanic membrane. In some cases they extended up to the
tympanic membrane. New plugs were made each time the ear was
occluded. Attenuations produced by ear plugs were estimated by
two methods that gave comparable results. In the first, the external
auditory canal was surgically opened near its junction with the
BINAURAL
DIRECTIONAL
bulla, and a probe tube microphone was sealed in the opening with
its tip near the tympanic membrane. The impulse response of a
high-frequency driver (Radio Shack 40- 13 1OB) was measured
with and without the ear plugged. The resulting frequency spectra
were subtracted showing that attenuation varied between 32-70
dB in the range of 4-32 kHz (the usable frequency range for the
measurements). At most frequencies, attenuations ranged between 40 and 60 dB, with lesser attenuations (32-40 dB) occurring over a narrow range of frequency that corresponded with a
notch in the spectrum from the unplugged ear (e.g., Musicant et
al. 1990). Ear-plug attenuation also was estimated by comparing
auditory brain stem response (ABR) thresholds to tone bursts
presented using the Polydax loudspeakers under unilateral and
bilateral ear-plug conditions. Attenuations were measured in
seven animals, and ranged between 55 and 70 dB at 4, 8, and 16
kHz, and between 35 and 55 dB at 2 kHz. Attenuation produced
at 1 kHz (presented using a Braun Output C loudspeaker with a
better low-frequency response than either the Polydax or Radio
Shack loudspeakers) was measured once using cochlear microphonic potential recordings at the round window, and it was
25 dB.
Thresholds to tone bursts (rise and fall ramps, 0.5 ms; duration,
3 ms) of 2, 4, 8, and 16 kHz were obtained from ABRs recorded
under unilateral ear-plug conditions. The ABRs were obtained a
few days before, or during, a recording session using a free-field
sound source located in the horizontal plane and aimed at the
opening of the unoccluded ear. When ABRs were recorded before
the experiment, the animal was anesthetized (sodium pentobarbital, ip) and placed in the sling with its lower jaw supported to hold
its head in roughly the same position as during a single-unit recording session. The ABR potentials were averaged over 500 or 1,000
stimulus repetitions. The level was varied in 5-dB steps, and threshold was defined as the lowest SPL that evoked a detectable response. Thresholds for stimulation of each ear in 20 normal adult
cats at 2, 4, 8, and 16 kHz were 23 t 7.2, 11 t 7.0, 8 t 7.9, and
18 -+ 5.7 (SD) dB SPL, respectively. Threshold disparities between
right and left ears calculated for each animal at each frequency
(n = 77) were 5 10 dB (3 t 3.6 dB). We rejected animals with
thresholds 220 dB above the normal mean or showing an interaural threshold disparity 2 15 dB.
Each animal was given a lethal dose of anesthetic at the end of
the experiment and perfused through the heart with a 10% solution of form01 saline. The brain was removed from the skull and
placed in a 30% sucrose form01 saline solution for cryoprotection
during histological processing. Brains were blocked in the plane of
the electrode penetrations and cut frozen into sections 50-pm
thick on a sliding microtome. Tissue sections were mounted on
glass slides and stained with cresyl violet. Electrode tracks were
reconstructed with the use of a drawing tube attached to a microscope. The location of single units in AI was confirmed from partial tonotopic maps obtained during each experiment.
Statistical treatment of data
Data sets consisted of single-unit responses to noise bursts that
varied in azimuth and level. Data sets were compared statistically
to determine whether treatment (ear plugging) had a significant
effect on the cell’s response and if so, whether a cell exhibited
binaural inhibition, binaural facilitation, or both. Cells typically
fired one spike, if any, and infrequently two or more spikes to a
noise burst. Nonparametric statistics were used because spike
counts were not normally distributed. One of two methods was
used depending on whether or not repeat data sets were obtained
using one treatment condition. If replications were available, an
analysis of variance (ANOVA) was used. Otherwise, a x2 test was
used.
CELLS
IN AI
2197
The x2 test was based on number of spikes evoked by each
stimulus repetition (response). To test the effect of ear plugging at
each azimuth, responses at all tested levels at that azimuth were
divided into plug and no-plug groups. Within each group the frequency of occurrence of responses consisting of zero, one, two,
etc., spikes were used to build a contingency table that was subjected to a x 2test (Beyer 1968; Siegel 1956). A Bonferroni correction (Glantz 1987) of the significance level ((w) was used to control
the error rate for multiple azimuth comparisons (corrected CY=
uncorrected a/number of comparisons = 0.05 /n).
An ANOVA was used to test for differences related to treatment
if repeated data sets were available for one or both treatment conditions. Data for the analysis included only those azimuth-level
combinations common to both treatment data sets. All responses
(average number of spikes per stimulus repetition) for each azimuth-level combination in the two treatment groups were pooled
together, ranked, and a three-factor ANOVA on the ranks was
performed (Glantz 1987). The three factors were treatment (T),
level (L), and azimuth (A), and the dependent variable was the
ranked response. The overall difference in response associated
with T, as well as the treatment X azimuth X level interaction
(TAL), the treatment X azimuth interaction (TA), and the treatment X level interaction (TL) were assessed.As this analysis was
only concerned with the effects of treatment, azimuth X level interactions and the overall effects of changing azimuth or level
within the same treatment are not discussed. T, TAL, TL, and TA
were considered significant when their respective probabilities
(PTY PTAL9P, , or PTL) were 10.05. Monaural and binaural data
sets were considered significantly different if PT 5 0.05. The interaction terms were used to test for azimuth- or/and level-dependent differences that were not reflected by a significant overall
mean difference associated with treatment. Post-hoc tests (x2 or
the one-tailed Fisher exact probability test) (Beyer 1968; Siegel,
1956 ) , based on the frequency of occurrence of responses consisting of zero, one, two spikes etc., were applied to data sets collapsed
across level and used to determine the azimuths at which responses were significantly different and whether monaural responses were greater or less than binaural responses (i.e., whether
the binaural interaction was inhibitory or facilitator-y). Post-hoc
tests were used to test further the significance of differences between monaural and binaural responses at each azimuth-level
combination. A Bonferroni correction was applied for all post-hoc
tests.
RESULTS
A set of noise bursts that varied in azimuth in the frontal
hemifield (in front of the interaural line) was presented to
each single unit. At each azimuth, noise bursts were presented over a broad range of SPLs. Responses to the stimulus set were displayed as an azimuth-level response area
( ALRA, e.g., no plug, Fig. 1A), a contour plot that represents response magnitude as a joint function of azimuth
and level. Because azimuth tuning is level dependent, an
azimuth function was calculated from an ALRA data set by
averaging over level to provide a level-independent measure of azimuth tuning [e.g., NP (no plug) D was derived
from the data in A]. Azimuth function modulation (difference between maximum and minimum values) was used as
an index of azimuth sensitivity, and cells were arbitrarily
classified as azimuth sensitive if modulation was 275%.
Neurons that met this criterion (e.g., NP, Fig. 1D) responded well to some levels at certain azimuths, but relatively poorly regardless of level at other azimuths (e.g.,
Fig. 1A).
F. K. SAMSON,
2198
---120
-90
-60
IPSI
-30
AZIMUTH
0
(DEGREE:;
P. BARONE,
60
90
CONTRA
J. C. CLAREY,
120
~-.I20
AND T. J. IMIG
-90
-60
IPSI
-30
AZIMUTH
30
60
90
CONTRA
(DiGREES)
120
90
C
70
-
NP
---*-Ip
.....0 .... cp
. . . . /-?%I
-120
-90
-60
IPSI
-30
AZIMUTH
0
(DEGREE&O
60
90
CONTRA
12
*-----“‘0
0.0 1
I
-10-l
-120
0
-90
. .. .. .
-60
IPSI
9 . .. .. ... .‘*_.._..
-30
0
AZIMUTH
1
90
60
30
120
CONTRA
(DEGREES)
F,$:::; ,,,/I
,,,,,
,111,
z
50
:::::
jz,~
-90
-60
IPSI
-30
AZIMUTH
0
(DEGREES)
30
60
90
CONTRA
,,
-90
-60
IPSI
,,
,,
-30
0
AZIMUTH
(DEGREES)
,I
30
.,,
90
60
CONTRA
RC. 1. M-type El cells with level-tolerant response borders. A-D: unit 89 1 l-l 1 [best frequency (BF), 12 kHz]. A-C:
azimuth-level response areas ( ALRAs) obtained using the plugging conditions at top lefi corners. An ALRA displays
response magnitude (% of maximum) as a joint function of azimuth and level. Small squares indicate stimulus azimuths and
levels in the data set. Iso-response contour lines represent 5%. 25%, 50%, and 75% of maximum response (diamonds).
Azimuth representation: median plane in front (0’) and behind (+ 180”) the head, contralateral, right (+90”) and ipsilateral, left (-90”) poles. ALRAs obtained under binaural (A), ipsilateral plug (B), and contralateral plug (C) conditions.
Maximum
responses were 1.O, 1.07, and 0.6 spikes/stimulus,
respectively, based on 15 stimulus repetitions. D: azimuth
functions for the binaural (NP), ipsilateral plug (IP), and contralateral plug (CP) conditions (numbers following such
abbreviations in the figures that follow indicate replications). Identical levels were used for the average values in each
azimuth function. Azimuth-level combinations at 0-dB SPL were excluded from the statistical tests if a unit was unresponsive at this level. A x2 test (corrected (Y = 0.05 / 7 = 0.007) showed that binaural responses were significantly smaller than
ipsilateral plug responses at -90” and - 120” (circled minus signs, D). E: unit 9 102-29 (BF, 9 kHz); F: unit 9 102-2 1 (BF,
8.5 kHz). Binaural ALRAs for 2 M-type EI cells; 10 stimulus repetitions in both cases. For both units, analysis of variance
(ANOVA) revealed significant overall ( Pr- ) , azimuth-dependent
(PTA), and level-dependent ( PTL ) effects of ipsilateral ear
plugging (9102-29: Pz = 0.0001, PTAL = 0.20, P,, = 0.001, and PTL = 0.0001; 9102-21: P, = 0.0001, P,, = 0.34, PTA =
0.0001, and PTL = 0.048). Post hoc tests on data combined across level (corrected 01 = 0.05/7 = 0.007) revealed that
binaural responses were significantly smaller than ipsilateral plug responses on the ipsilateral side. Binaural responses did not
exceed ipsilateral plug responses at any azimuth tested. Post hoc tests on data for individual azimuth-level combinations
(corrected LY = 0.05/28 = 0.0018) revealed azimuth-level combinations at which binaural responses were significantly
smaller than the ipsilateral plug responses (circled minus signs).
The effect of ear plugging on the responses of 131 azimuth-sensitive cells was studied. The responses of 42 of
them were too unreliable to characterize. The remaining 89
cells were classified as MD (30%, 27/89) (Samson et al.
1993) or as BD (70%, 62/89), and this latter group is described below.
Best frequency (BF), defined as the midpoint of the fre-
quency range that excited a cell at lo-20 dB above lowest
threshold, was determined at a preferred azimuth (azimuth
function value 2 75% of maximum), which was often the
maximal azimuth (corresponding to the maximum response in the ALRA data set). BFs of BD cells ranged between 5.0 and 24 kHz. All BD cells discharged at short
latencies (8-25 ms) after the stimulus onset, and under cer-
BINAURAL
DIRECTIONAL
tain stimulus conditions, a few of them (4/ 62) also responded at longer latencies (48-98 ms). These late responses were not included in the analysis, but their inclusion would not have altered any of our conclusions.
Electrode track reconstructions allowed identification of
the recording sites for 58% of the BD sample ( 36/62 cells),
and a majority (30/ 36) was located in layers III and IV.
The remainder was located in layers II, V, and VI.
If a cell was determined to be azimuth sensitive for binaural (without ear plugs) stimulation, ALRAs also were
obtained for monaural (unilateral ear plug) stimulation. If
time permitted, ALRAs were obtained for monaural stimulation of each ear, and additional binaural and monaural
ALRAs were obtained to test for reliability of the response.
Binaural interactions were inferred by statistically comparing binaural and monaural responses to the same azimuths
and levels of noise stimulation. A significantly larger binaural response than either monaural response was interpreted as evidence for binaural facilitation. A significantly
smaller binaural than monaural response was taken as evidence for binaural inhibition. Cells that exhibited binaural
facilitation composed 65% (40/62) of the BD sample, and
many of these exhibited mixed interactions, i.e., binaural
facilitation at some azimuth-level combinations and binaural inhibition at others. Binaural inhibition in the absence of binaural facilitation was exhibited by 35% (22/ 62)
of the BD sample. Most were EI cells that received excitatory input (discharge of action potentials) from one ear
(excitatory ear) and inhibitory input from the other (inhibitory ear).
For each cell, a level function was obtained at the maximal azimuth. In most cases,response magnitude was a nonmonotonic function of level, i.e., as level increased from
threshold, response magnitude increased to a maximum
and then decreased (e.g., Fig. 3F). Each cell was tested
using levels that varied from near threshold up to 80 dB
SPL except for some nonmonotonic cells that ceased responding at lower levels. The decrease in response magnitude at the highest level tested (nonmonotonic strength)
varied from 0% ( e.g., NP2, Fig. 11D) to 100% ( e.g., Fig.
30). For descriptive purposes, level functions with nonmonotonic strengths of >50% were classified as NM-type
functions, and those with nonmonotonic strengths 150%
were classified as M-type functions. Under binaural conditions, 60% of the sample (37/62) exhibited NM-type level
functions, including 8 1% ( 17/2 1) of the EI sample and
50% (20/40) of the facilitatory sample.
EI cells responded vigorously throughout much or all of
one frontal quadrant (preferred side) and relatively poorly
throughout the other quadrant (nonpreferred side, e.g., Fig.
1A). In each case, plugging the ear on the nonpreferred side
caused an increase in responsiveness at locations where the
cell had responded poorly to binaural stimulation and consequent loss of azimuth sensitivity. From this it was inferred that the ear on the preferred side provided excitatory
input, the ear on the nonpreferred side provided inhibitory
input, and that azimuth sensitivity depended upon binaural
stimulation. The contralateral quadrant was preferred by
the majority (86%, 18/21).
An example of an M-type EI cell that was studied with
CELLS
IN AI
2199
unilateral plugging of each ear is shown in Fig. 1, A-D.
ALRAs were obtained for each of three plugging conditions
(A : no plug, B: ipsi plug, C: contra plug), and the corresponding azimuth functions are labeled NP, IP, and CP
(D). Under binaural conditions, a response border can be
identified ( no plug, A; NP, D) as a steep gradient in response magnitude that occurred between O” and -30° azimuth. The location of the response border was relatively
invariant over a broad range of levels ( level tolerant) as
reflected in near-vertical, near-parallel, 50% and 75% isoresponse contour lines (A).
Monaural contralateral stimulation, simulated by ipsilatera1 plugging, was inferred to be excitatory because it produced vigorous responses to sound sources located
throughout the entire frontal hemifield (ipsi plug, B; IP,
D). Thresholds (defined in each ALRA by the 5% iso-response contour line) were lowest contralaterally, presumably reflecting diffraction of high-frequency sound by the
head and pinna (Irvine 1987; Musicant et al. 1990). For
most frequencies, direction-dependent acoustic gain at the
tympanic membrane (TM) is maximum within the frontal
quadrant ipsilateral to that ear, and it decreases more or less
monotonically as the sound source is displaced through the
contralateral frontal quadrant towards the contralateral
ear. Stimulation of the ipsilateral ear was inferred to provide inhibitory input because the cell was less responsive in
the ipsilateral quadrant under binaural conditions than
under ipsilateral plug conditions [compare NP and IP (D),
statistical comparisons are described in the figure legends].
Monaural ipsilateral stimulation (contra plug, C; CP, D)
was ineffective at most azimuth-level combinations, but a
response did occur at 80-dB SPL in the contralateral quadrant. This may have been a result of sound reaching the
contralateral ear through the plug. The lowest threshold to
contralateral ear stimulation was ~0 dB SPL (B) , so that
even with a plug producing the maximum attainable attenuation of 70 dB, an 80-dB SPL sound in the free field would
still achieve a level 10 dB above the cell’s threshold. Furthermore, if sound reaching the ipsilateral ear were the source of
excitatory input at high levels, then acoustic gain should be
greatest and consequently thresholds lowest at ipsilateral
directions. However, thresholds were lowest in the contralateral field, suggesting that sound reaching the contralatera1 ear was driving the cell. Taken together, ear plugging
suggests that stimulation of the contralateral but not the
ipsilateral ear excited the neuron.
Two additional examples of M-type, contralateral-preferring EI cells with level-tolerant response borders are illustrated in Fig. 1, E and F. Each cell responded nonselectively throughout the entire frontal field to monaural contralateral stimulation (ipsilateral plug) with lowest thresholds
in the contralateral quadrant. The circled minus signs in the
ALRAs indicate azimuth-level combinations at which the
binaural response was significantly smaller than the monaural contralateral response, showing that ipsilateral ear
stimulation had an inhibitory effect. Significant inhibitory
effects of ipsilateral ear stimulation were found at ipsilateral
and midline locations, but the responses at most contralatera1 directions were not significantly different. These findings showed that the cells received excitatory input from
2200
F. K. SAMSON,
80
P. BARONE,
J. C. CLAREY,
NO PLUG 3
60
.
-20
8932-l
-"-"-
-90
2
-60
-30
AZIMUTH
IPSI
'1'
0
-1.
30
-I-
-'
60
90
CONTRA
(DEGREES)
80,
1
$20
0
I
-60
-90
IPSI
-30
AZIMUTH
0
30
60
I
NP 1
-
NP2
CPI
IP
. ..m.*....
!!j 0.8
---&mm-
5
I
90
CONTRA
(DEGREES)
0.6
. . . . I .e,
. . . .
-
CP2
NP3
0.0
-90
IPSI
-60
-30
AZIMUTH
0
30
(DEGREES)
60
90
CONTRA
FIG. 2. An NM-type EI cell (8932- 12; BF, 8 kHz) with similar monaural and binaural level tuning. A and B: ALRAs obtained under binaural
and contralateral plug conditions, respectively. Maximum responses were
1.1 and 1.3 spikes/stimulus,
respectively; 10 stimulus repetitions. C: azimuth functions. The cell was unresponsive with the ipsilateral ear plugged.
An ANOVA revealed significant effects of contralateral plugging (Pr =
0.025, PTAL= 0.026, PTA= 0.0008, and PTL = 0.0 14). Post hoc tests on
data combined across level (corrected CY= 0.05 /7 = 0.007) revealed that
binaural responses were significantly smaller than contralateral plug responses on the contralateral side. No other significant differences were
found. Post hoc tests on data for individual azimuth-level combinations
(corrected a! = 0.05 / 2 1 = 0.0024) revealed azimuth-level combinations at
which binaural responses were significantly smaller than contralateral plug
responses (circled minus signs, A ) .
the contralateral ear and inhibitory input from the ipsilatera1 ear.
Most NM-type EI cells were contralateral preferring, but
a few were ipsilateral preferring, and one such example is
shown in Fig. 2. The cell was tested on three different occa-
AND
T. J. IMIG
sions under binaural conditions (e.g., Fig. 2: no plug 3 in A
and NP l-NP 3 in C) and was found to be azimuth sensitive and ipsilaterally preferring each time. It did show a
continuing decrease in responsiveness throughout the test
period (e.g., Fig. 2: NP I-NP 3 in C).
Monaural stimulation of the ipsilateral ear (Fig. 2: contra
plug 2 in B and CP 1 and CP 2 in C) caused the cell to
respond nonselectively to azimuth. Monaural stimulation
of the contralateral ear did not produce a response (IP, Fig.
2C). Responses to contralateral directions were significantly smaller to binaural than to ipsilateral monaural stimulation ( circled minuses, Fig. 2A) indicating that stimulation of the contralateral ear was inhibitory. There was no
significant difference between responses to binaural and
monaural ipsilateral stimulation at midline and ipsilateral
directions (0” to -9OO).
Binaural and monaural level tuning at preferred azimuths was similar for most EI cells, including those with
M-type level tuning (e.g., Fig. 1) and NM-type level tuning
(e.g., Fig. 2) (for an example of a contralateral-preferring
cell with similar properties, see Fig. 8 in Samson et al.
1993). On the other hand, five EI cells exhibited similar
binaural and monaural responses at levels near threshold,
but at higher levels, they were less responsive to binaural
than to monaural stimulation. An example of a contralateral-preferring cell with such properties is illustrated in Fig.
3A. Monaural contralateral stimulation (ipsi plug, Fig. 3B)
caused the cell to respond nonmonotonically and nonselectively to sound direction with lowest thresholds in the contralateral quadrant, indicating that the contralateral ear
provided nonmonotonic excitatory input. The plug was removed, the cell was tested without plugs two more times,
and its responses were similar to the first binaural response
(Fig. 3, A and C). The cell was more responsive to monaural contralateral stimulation (ipsilateral plug) than under
binaural conditions at most azimuths (significant differences indicated by circled minus signs, Fig. 3C), indicating
that stimulation of the ipsilateral ear produced inhibitory
input. The inhibition was most effective at ipsilateral sound
directions and gradually diminished toward the contralatera1 pole.
Level tuning within the contralateral quadrant was
narrower to binaural (no plug 1, Fig. 3A) than to monaural
contralateral stimulation (ipsi plug, Fig. 3 B) showing that
inhibition from the ipsilateral ear sharpened the cell’s level
tuning. Thresholds for binaural and monaural contralateral
stimulation were similar, suggesting that the binaural response near threshold depended exclusively upon monaural stimulation of the contralateral ear. In contrast, the
decline in responsiveness with increasing level (upper response cutoff) occurred at lower levels to binaural than to
monaural contralateral (ipsilateral plug) stimulation showing that inhibition from the ipsilateral ear lowered the upper response cutoff. This effect also can be seen by comparing level functions obtained within the contralateral quadrant under binaural and ipsilateral plug conditions. At 30’
and 60’ (Fig. 3, D and E), level functions exhibited no
differences at lower levels (e.g., O-20 dB) that could be attributed to ear plugging, but responsiveness at higher levels
( 30 and 40 dB in Fig. 3 D, 40 dB in Fig. 3E) was much less
BINAURAL
0
DIRECTIONAL
m
n
g
si
s
E
2
0
-90
.
8944- 1.7
.‘,*.,*,,..,,.,,,’
-60
IPSI
-30
AZIMUTH
y”
$
.
.
.
0
30
60
(DEGREES)
2201
-+
D 0.5
NO PLUG 1
n
CELLS IN AI
AT
30”
0.4-
-
NPl
0.3 -
-
NP2
NP3
0.2 -
0.1 -
90
30
SPL
CONTRA
50
(dB)
AT
-90
-60
IPSI
-30
AZIMUTH
0
30
(DEGREES)
60
-10
90
-
10
30
CONTRA
AZIMUTH
--Q--,
-
NPl
IP
NP2
-
NP3
70
90
(dB)
0.6
AT
90”
AZIMUTH
-
NPl
-
NP2
NP3
NPl
0
0.0
-90
IPSI
60”
50
SPL
F
AZIMUTH
-60
-30
AZIMUTH
0
30
(DEGREES)
60
90
CONTRA
0.0
-10
10
30
\L
50
SPL
70
90
(dB)
FIG. 3. An NM-type EI cell (8944-17; BF, 9 kHz) with binaural level tuning that reflected a combination of nonmonotonic monaural excitatory input and binaural inhibition. A and B: ALRAs obtained under binaural and ipsilateral plug
conditions. Maximum responses were 0.55 spikes/stimulus in both cases; 20 stimulus repetitions. C: azimuth functions
obtained under different treatment conditions. D-F: level functions obtained at 30”, 60”, and 90’ of azimuth, respectively.
An ANOVA revealed that the overall effect of plugging the ipsilateral ear was significant and that the effect varied with level
(PT = 0.0001, P*AL = 0.22, PTA = 0.11, and P, = 0.000 1). Post hoc tests on data combined across level (corrected a =
0.05 /7 = 0.007 ) revealed that binaural responses were significantly smaller than ipsilateral plug responses at most azimuths
(circled minus signs, C) . Post hoc tests on data for individual azimuth-level combinations (corrected CY= 0.05 / 35 = 0.00 14)
failed to show significant differences between binaural and monaural responses.
under binaural than ipsilateral-plug conditions. Binaural
and ipsilateral-plug level functions were similar at 90’ (Fig.
3 F), showing that ipsilateral inhibition did not affect level
tuning at this location. In summary, the nonmonotonic
level tuning that this cell exhibited under binaural conditions depended upon binaural inhibition and nonmonotonic excitatory input from the contralateral ear.
Another cell whose level tuning was narrower to binaural
than to monaural stimulation is shown in Fig. 4A. In response to binaural stimulation, it was selective to sound
directions near the contralateral pole. The ipsilateral ear
was then plugged (ipsi plug, Fig. 4B). The cell became nonselective to azimuth and significantly more responsive at all
azimuths than it was under binaural conditions. This
showed that the contralateral ear provided excitatory input,
that the ipsilateral ear provided inhibitory input, and that
azimuth sensitivity depended upon binaural stimulation.
Furthermore the cell was more strongly nonmonotonic and
narrowly tuned to level under binaural than under ipsilateral-plug conditions, as can be seen by comparing level
functions obtained at 90* (Fig. 4C). Responses to low SPLs
(O-20 dB) were similar under both conditions, but for SPLs
at 40 dB and higher, the binaural response was significantly
smaller than the monaural response.
Responses to unilateral ear plugging of each ear were obtained for 4/2 1 of the cells classified as EI (e.g., Fig. 1,
A-D), and in each case, unilateral plugging showed that the
ear on the preferred side was excitatory and the other was
not. For the remainder ( 17 /2 1 ), responses were obtained
only with plugging of the ear on the nonpreferred side, but
2202
F. K. SAMSON,
90
A .
NO PLUG
P. BARONE,
2 m
m
70-
g50Y
ii
cn 301 o-
m
n
m
8
m
w
n
d
8
l
n
1
/
n
m
T
-180
- 120
-60
AZIMUTH
0
120
60
180
(DEGREES)
J. C. CLAREY,
AND T. J. IMIG
not with plugging of the other ear (e.g., Fig. 3). In this
group of cells, comparison of binaural and unilateral earplug ALRAs were sufficient to demonstrate inhibition from
one ear and excitation from the other. Nevertheless if monaural stimulation of each ear was excitatory, we would not
have detected it. One cell (classified as EE/I), which is not
included in the EI sample, exhibited such a response. It was
excited by monaural stimulation of each ear and exhibited
binaural inhibition and at some azimuths, binaural responses were smaller than either monaural responses. So
we cannot rule out the possibility that some cells classified
as EI on the basis of plugging only one ear may have been
bilaterally excited.
Facilitatory interactions
WY
B IPSI
PLUG
70-
g50u
;301 o-
-1 80
C
2
-120
-60
AZIMUTH
AT
90”
0
60
(DEGREES)
AZIMUTH
-
NPI
IP 1
w-m.*--.
---e-m,
10
30
50
SPL
Midline cells
IP 2
NP2
-
-10
180
120
70
Cells exhibiting facilitator-y interactions exhibited a rich
diversity of response profiles. Midline (22.5%, 9 /40) and
lateral field (LF; 77.5%, 3 l/40) cells were distinguished on
the basis of differences in azimuth selectivity. The azimuth
functions of midline cells had maximum values (a peak) at
locations 5 15 * from the midline (0’ azimuth) and reached
minima of <25% of maximum on both sides of the peak in
front of the interaural line (Figs. 5 and 6). LF cells were
selective to lateral locations (e.g. Figs. 7- 13), and there
were slightly more ipsilateral ( 5 5%, 17 / 3 1) than contralatera1 (45%, 14/ 3 1) preferring cells in the sample. LF cells
were distinguished from midline cells by azimuth functions
that decreased to ~25% of maximum only on one side of
the peak in the frontal field ( 30 / 3 1) or by an azimuth function peak located > 15 * from the midline ( 1 / 3 1, Fig. 7A ) .
Half of the facilitatory sample exhibited NM-type level
functions, including cells with midline (5 /9) and LF ( 15 /
3 1) azimuth preferences.
90
(dB)
FIG. 4. An NM-type EI cell (922 l- 11; BF, 7.8 kHz) with binaural level
tuning that depended predominantly upon binaural inhibition. ,4 and B:
ALRAs obtained under binaural and ipsilateral plug conditions, respectively. Maximum responses were 1.3 and 1.2 spikes/stimulus, respectively; 10 stimulus repetitions. C: level functions at 90’ azimuth. Replicated data were available only for azimuths from 0’ to 90”, and an ANOVA was calculated for that azimuth range to test the effect of plugging the
ipsilateral ear. This analysis revealed a significant overall ear plugging effect and that the effect was azimuth and level dependent ( PT = 0.0001,
PTAL= 0.65, PTA= 0.025, and PT,y= 0.000 1). Post hoc tests on data
combined over azimuths (corrected CY= 0.05/5 = 0.01) revealed that
binaural responses were significantly smaller than ipsilateral plug responses at 40., 60-, and 80-dB SPL (circled minus signs, C) showing the
inhibitory effect of ipsilateral stimulation at these levels. There were no
differences at 0- or 20-dB SPL. Post hoc tests on data for individual azimuth-level combinations (corrected CY= 0.05 / 20 = 0.0025) failed to show
significant differences between binaural and monaural responses.
Each midline cell was tested with unilateral plugging of
each ear and was found to respond poorly, if at all, to monaural stimulation. An example of an M-type midline cell
appears in Fig. 5A. The cell was selective for central field
directions and also responded weakly to high levels at the
contralateral pole. ALRAs were obtained under binaural
conditions on four different occasions, and the resulting
azimuth functions are shown in Fig. 5 D . The cell’s azimuth
selectivity and responsiveness were relatively stable for the
entire period that it was studied. With either the contralatera1 (Fig. 5 B) or ipsilateral (Fig. 5C) ear plugged, the cell
responded only at relatively high levels on the side of the
plugged ear. After removing the plugs from each ear, the
cell regained its midline preference. These data show that
this cell’s midline azimuth preference derived from binaural facilitation. Three other M-type midline cells had similar characteristics. One was nearly identical to that illustrated in Fig. 5, and with either ear plugged, it responded
weakly at high levels on the side of the plugged ear. The
other two cells were completely unresponsive with either
ear plugged.
Two examples of NM-type midline cells are shown in
Fig. 6, A and B. The cell in Fig. 6A responded only to
locations near the midline, and it was completely unrespon-
BINAURAL
DIRECTIONAL
CELLS IN AI
NO PLU
CONTRA
2203
: .
PLUG
e
10
4
9 1 04 -
-10
2.2
I
-60
-90
IPSI
n
I
-30
AZIMUTH
m
I
0
(DEGREES)
.
I
30
n
I
I
1
60
90
CONTRA
-10
I
- 90
IPSI
1’-
1.6
!i
2
t
-60
-30
AZIMUTH
I
0
(DEGREES)
I
30
I
60
90
CONTRA
NPI
_-
NP2
-
NP3
-
NP4
0.8
W
Y
1
z 0.4
cn
-1
-90
-60
IPSI
-30
AZIMUTH
0
(DEGREES)
30
60
90
CONTRA
0.0
90
IPSI
-60
-30
AZIMUTH
0
30
(DEGREES)
60
90
CONTRA
FIG. 5. An M-type midline cell ( 9 104-22; BF, 12 kHz) showing binaural facilitation. A-C: ALRAs obtained using the
plugging condition shown in the top left corner. Maximum responses were 2.2,0.4, and 0.8 spikes/stimulus, respectively; 10
&imului repetitions. D : azimuth functions.
sive with either ear plugged. Figure 6B shows a cell that
responded over a broader level range than the example
shown in Fig. 6A. It was most responsive at locations near
the midline, but also responded weakly in a broad range of
levels throughout the contralateral quadrant. It responded
very weakly with unilateral plugging of either ear (Fig. 6C)
showing that its binaural response was a product of strong
binaural facilitation.
LF cells
Each LF cell was tested with unilateral plugging of the ear
on the nonpreferred side, and most (25 /3 1) also were
tested with unilateral plugging of the other ear. LF cells
exhibited considerable variation in strength of monaural
excitation. Two NM-type cells were unresponsive to monaural stimulation (Fig. 7). Each was tested with binaural
stimulation following ear plugging to ensure that the unit
had not been lost. None of the M-type LF cells in our sample was completely unresponsive to monaural stimulation,
although several responded poorly to it. Most of the remaining LF cells were excited exclusively or predominantly
by the ear on the preferred side. Plugging of the other ear
caused an increase in responsiveness on the nonpreferred
side and a decrease in responsiveness on the preferred side
showing that the binaural response was a result of mixed
interactions. Examples of LF cells with this type of response
are shown in Figs. 8, 9, 11, and 13.
A few LF cells responded securely to monaural stimulation, and their level tuning at preferred azimuths was similar for binaural and monaural stimulation (e.g., Fig. 8 ) .
Under binaural conditions, the cell was ipsilateral prefer-
ring (no plug 1, Fig. 84. It received nonmonotonic ipsilatera1 excitatory input (contra plug 2, Fig. 8 B; CP 1 and CP
2, Fig. 8C) and was not excited by monaural contralateral
stimulation ( IP, Fig. 8C). The binaural response was significantly smaller in the contralateral quadrant and significantly larger in the ipsilateral quadrant (Fig. 8C, circled
minus and plus signs, respectively) than the monaural ipsilateral response thus revealing mixed binaural interactions.
Ear plugging had little effect on the threshold or breadth of
level tuning at preferred azimuths. This shows that monaural ipsilateral input could, in large part, account for binaural level tuning.
An M-type LF cell that exhibited similar monaural and
binaural level tuning at preferred azimuths is shown in Fig.
9. This cell was tested under binaural conditions on three
separate occasions and exhibited similar ALRAs each time
(no plug 1, Fig. 9A ; NP l-NP 3, Fig. SC). It responded
vigorously over a broad range of levels in the contralateral
quadrant and was responsive only at high levels in the ipsilateral quadrant. The ipsilateral ear was plugged on two
separate occasions. With the plug, the cell responded nonselectively to azimuth with lowest thresholds contralaterally ( ipsi plug 1, Fig. 9 B ; IP 1 and IP 2, Fig. SC) showing
that monaural stimulation of the contralateral ear excited
the cell. The cell was tested with ipsilateral monaural stimulation on one occasion and was found to respond weakly
and sporadically over a broad range of azimuths and levels,
as reflected in the azimuth and level functions (CP, Fig. 9,
C and D). Comparison of azimuth functions (Fig. 9C) obtained to binaural (NP 1-NP 3) and contralateral monaural ( IP 1 and IP 2) stimulation revealed binaural facilita-
F. K. SAMSON,
2204
P. BARONE,
tion in the contralateral quadrant and binaural inhibition
in the ipsilateral quadrant. The effect is shown in greater
detail in Fig. 9A where the circled plus signs indicate azimuth-level combinations at which the binaural response
was significantly greater than the monaural contralateral
response and the circled minus signs indicate azimuth-level
combinations at which the binaural response was significantly smaller than the monaural ipsilateral response. Level
functions for monaural (IP) and binaural (NP) stimulation
obtained at 30’ azimuth (Fig. 90) reveal that, within the
limits of resolution of the measurements, thresholds and
the monotonic form of the functions appear similar.
90
J. C. CLAREY,
4
-10
n
I
-90
-60
IPSI
NO PLUG
A
AND T. J. IMIG
4
n
I
8
I
I
-30
AZIMUTH
n
0
I
30
60
CONTRA
(DEGREES)
90
9
B
7
n
m
n
I
I
I
B
8940-22
-1
. w -90
I)
-60
-30
AZIMUTH
IPSI
I
I
0
30
I
60
90
CONTRA
(DEGREES)
1 o4
5.0
-joy---8 9 4 3 - -,-90
IPSI
-60
n
8
m
I
I
I
-30
0
AZIMUTH
(DEGREES)
30
8
I
60
I
90
CONTRA
FIG. 7. Two NM-type lateral field (LF) cells that were unresponsive to
monaural stimulation of either ear. A : unit 8940- 18 (BF, 14 kHz); 20
stimulus repetitions. B: unit 8943-50 (BF, 17 kHz); 10 stimulus repetitions. Maximum responses were 0.6 and 1.4 spikes/stimulus, respectively.
-10’
-90
8943-5.6
v -
I
-60
*
IPSI
=
’
I
0
”
I
30
-
-
I
-
60
’
90
CONTRA
(DEGREES)
8943-56
NP
-60
IPSI
I
-30
AZIMUTH
-
-90
-
-30
AZIMUTH
0
30
(DEGREES)
60
90
CONTRA
FIG. 6. Two NM-type midline cells showing binaural facilitation. A:
unit 8940-22 (BF, 17 kHz) did not respond with unilateral plugging of
either ear. Maximum response was 0.3 spikes / stimulus; 20 stimulus repetitions. B: unit 8943-56 (BF, 17 kHz) responded weakly with unilateral ear
plugging. Maximum response was 1.4 spikes/stimulus. C: azimuth functions for unit 8943-56; 10 stimulus repetitions.
The majority of LF cells exhibited monaural and binaural level tuning at preferred azimuths that differed in
threshold, function form (M-type or NM-type), or both.
An M-type cell that exhibited lower thresholds to binaural
than to monaural stimulation is shown in Fig. 10. It responded weakly to monaural contralateral ear stimulation
in a broad range of azimuths (ipsi plug, Fig. 1OC). It also
responded weakly to monaural ipsilateral ear stimulation at
high levels near the contralateral pole (contra plug, Fig.
lOB), although this response could represent acoustic leakage through the plug. Comparison of azimuth functions
obtained under different plugging conditions ( Fig. 1OE)
revealed strong facilitation throughout the contralateral
quadrant. Level functions, obtained at the maximal azimuth (O”, Fig. 10 D), show that thresholds to binaural stimulation (NP) were 220 dB and as much as 40 dB lower than
thresholds to monaural stimulation.
An M-type cell for which binaural thresholds were only
slightly lower than monaural thresholds is shown in Fig. 11.
Under binaural conditions (Fig. 11 A), the cell responded to
a broad range of levels in the ipsilateral quadrant and at
high levels in the contralateral quadrant. Monaural ipsilatera1 stimulation (contra plug, Fig. 11 B) was excitatory,
causing the cell to respond throughout both quadrants of
the frontal field with lowest thresholds on the ipsilateral
side. Monaural contralateral stimulation (IP, Fig. 11 C)
produced no response, Comparison of azimuth functions
BINAURAL
DIRECTIONAL
I
90
NO PLUG
A 70- -
-lo!
-90
I
I
I
1
I
1
-30
0
30
60
90
AZIMUTH
B70-
PLUG
CONTRA
CONTRA
(DEGREES)
2
l
.
-IO!
I
-60
-90
AZIMUTH
IPSI
C
I
930
I
0
I
I
30
I
60
90
CONTRA
(DEGREES)
0.5
-
NPI
0.4
0.3
0.2
IL
ii
m
0.1
8
0.0
-60
-90
IPSI
-30
AZIMUTH
0
(DEGREES)
30
60
2205
B). Values of monaural and binaural level functions (Fig.
3
-60
IPSI
90
89324
1
CELLS IN AI
90
CONTRA
FIG. 8. An NM-type LF cell with similar binaural and monaural level
tuning ( 8932- 13; BF, 8.5 kHz). A and B: ALRAs obtained under binaural
and contralateral plug conditions. The cell was unresponsive with the ipsilateral ear plugged. Maximum responses were 1.1 and 0.8 spikes/stimulus,
respectively; 10 stimulus repetitions. C: azimuth functions. An ANOVA
showed significant interaction terms indicating that the effect of contralatera1 ear plugging depended on azimuth and level (pT = 0.98, PTAL =
0.0009, PTA = 0.000 1, and PTL = 0.013). Post hoc tests on the data combined across levels revealed mixed interactions (corrected M = 0.05 /7 =
0.007 ) . Binaural responses were significantly smaller than contralateral
plug responses at 30’ and 60° (circled minus signs, C) and significantly
larger than contralateral plug responses at -60° and -90’ (circled plus
signs). Post hoc tests on data for individual azimuth-level combinations
(corrected (Y = 0.05/28 = 0.0018) failed to show significant differences
between binaural and monaural responses.
obtained under binaural and monaural conditions (Fig.
11 C) revealed binaural facilitation in the ipsilateral quadrant and binaural inhibition in the contralateral quadrant.
This unit exhibited somewhat lower binaural than monaural thresholds at -3O* and 0’ azimuth (Fig. 11, A and
11 D) are most similar at higher SPLs (40-80 dB), and
most different at 20 dB where facilitation is strongest.
An example of an M-type cell that received bilateral
monaural excitation is shown in Fig. 12A. Unlike most LF
cells, it received stronger monaural excitation from the ear
on the nonpreferred side. It responded vigorously over a
broad range of levels within an azimuth range that included
the midline and the adjacent part of the ipsilateral frontal
quadrant and was also responsive at high levels elsewhere.
With unilateral plugging of either ear, the cell responded
throughout both quadrants of the frontal field (Fig. 12, B
and C), showing that it received excitatory input from each
ear. The azimuth functions (Fig. 12E) showed that facilitation was important in forming the response peak, as binaural responses were significantly greater than monaural
responses at preferred azimuths (circled plus signs, Fig.
12E). Both ears produced monaural excitation, and the
binaural response was smaller than the monaural contralatera1 response at 60* (IP, circled minus sign in Fig. 12E).
This shows that stimulation of the ipsilateral ear produced
both excitation and inhibition similar to responses of the
EE/ I cell mentioned earlier. Monaural and binaural level
functions that were obtained at the maximal azimuth (O”,
Fig. 12 D) were quite different. At 20., 40-, and 60-dB SPL,
the binaural response was greater than the response to monaural stimulation of either ear and also greater than the sum
of the monaural responses. The threshold for monaural
stimulation of the ipsilateral ear (CP) was higher than the
binaural threshold. Although the thresholds to binaural and
contralateral monaural stimulation (IP) may be similar,
the forms of the level functions were quite different.
Monaural and binaural level tuning was similar for a few
NM-type LF cells (e.g., Fig. 8), but very different for the
vast majority, as illustrated by two examples in Fig. 13. In
both cases, the ear on the preferred side was excitatory. The
first cell ( Fig. 13A ) was responsive throughout the contralatera1 quadrant, with the strongest (primary) response occurring at the midline. It also exhibited a relatively vigorous
( secondary) response at +90” at higher levels. Many cells in
this group exhibited a primary response at relatively low
levels in the central part of the frontal field and a secondary
response at higher levels near a lateral pole. Monaural ipsilateral stimulation was not excitatory (CP, Fig. 13C). Monaural contralateral stimulation (ipsi plug, Fig. 13 B) produced M-type excitation throughout most of the frontal
field with lowest thresholds in the contralateral quadrant.
Similarity of binaural ALRAs obtained before and after ear
plugging (not illustrated) revealed that the cell’s response
was quite stable over the time that it was tested.
Comparison of the binaural and monaural responses revealed mixed binaural interactions. Binaural responses
(Fig. 13A) to ipsilateral directions (-30*, -6O*, -90')
were significantly smaller than those obtained under ipsilatera1 plug conditions (Fig. 13 B), and binaural responses to
midline and contralateral directions (O”, 60”, 90* ) were
significantly greater than those obtained under ipsilateral
plug conditions. The nonmonotonic
level functions (Fig.
13C) obtained at the maximal azimuth show that facilitation was level dependent. Responses at 20 and 40 dB were
much larger under binaural than ipsilateral plug conditions
2206
F. K. SAMSON,
90
I
P. BARONE,
J. C. CLAREY,
AND T. J. IMIG
1
. . ..I.
mm...
CP
NP3
41
8936-6
n
I
-60
-10
-90
IPSI
B
9 0
IPSI
PLUG
I
-30
AZIMUTH
I
0
(DEGREES)
I
30
1
I
i
90
60
CONTRA
u.u
-901
IPSI
I
40
40
AZIMUTH
-
3'0
d
(DEGREES)
6'0
9'0
CONTRA
NPI
7
1
-10
AT
I
-60
I
-90
IPSI
I
-30
AZIMUTH
I
0
(DEGREES)
I
30
I
I
60
90
CONTRA
-10
10
30”
AZIMUTH
30
-
50
SPL
70
9
(cm)
FIG. 9. An M-type LF cell with similar binaural and monaural level tuning (8936-04;
BF, 7 kHz). A and B: ALRAs
obtained under binaural and ipsilateral plug conditions. Maximum responses were 1.35 and 1.2 spikes/stimulus, respectively; 20 stimulus repetitions. C: azimuth functions. D : level functions at maximal ( 30” ) azimuth. An ANOVA revealed an
azimuth-dependent ear plugging effect ( PT = 0.82, P,, = 0.13, PTA= 0.0001, and PTL= 0.083). Post hoc tests on the data
combined across levels revealed mixed interactions (corrected a = 0.05 / 7 = 0.007 ) . Binaural responses were significantly
smaller than ipsilateral plug responses on the ipsilateral side and significantly larger than ipsilateral plug responses on the
contralateral side. Post hoc tests on data for individual azimuth-level combinations (corrected CY= 0.05 / 28 = 0.00 18 )
revealed azimuth-level combinations at which binaural responses were significantly smaller (circled minus signs, A ) and
larger than ipsilateral plug responses (circled plus signs, A and II).
revealing binaural facilitation at those levels, but there was
no evidence of facilitation at 60 or 80 dB.
The ALRA of another contralateral-preferring,
NM-type
cell (Fig. 13 0) was characterized by a primary response at
low levels located at 30’ azimuth and a secondary response
at higher levels at the contralateral pole. Monaural contralateral stimulation produced M-type excitation (ipsi plug 1,
Fig. 13 E; IP 1 and IP 2, Fig. 13 F). Comparison of binaural
and monaural ALRAs ( Fig. 13, D and E) revealed binaural
inhibition in the ipsilateral quadrant and binaural facilitation in the contralateral quadrant (Fig. 13 D, statistically
significant differences, circled minus signs, inhibition; circled plus sign, facilitation). Comparison of level functions
obtained at the maximal azimuth under binaural and monaural conditions (Fig. 13 F) showed that binaural facilitation occurred at 40-dB SPL and binaural inhibition occurred at 80-dB SPL. There was not much difference between the monaural and binaural thresholds at most
preferred azimuths for either cell, but the form of the monaural and binaural level functions was very different.
M/B ratio
The ratio of monaural to binaural responsiveness (M/B
ratio) was used to quantify the relative effectiveness of
monaural stimulation for each cell (see legend of Fig. 14).
For EI cells, monaural responsiveness of the ear on the preferred side was compared with binaural responsiveness, and
M/B values varied between 0.63-1.93, with an average of
1.18 (Fig. 14A). If responsiveness at preferred azimuths
were exclusively a function of input from the excitatory ear,
then an average M/B value of 1.O would be expected. If
binaural inhibition caused decreased responsiveness at preferred azimuths, as was the case in some cells, then M/B
ratios > 1.0 would be expected. Midline cells were either
completely unresponsive to monaural stimulation at the
preferred azimuth ( 6 / 9) or responded weakly as indicated
by low M/B ratios ( mean 0.05, Fig. 14 B) . Lateral field cells
exhibited considerable variation in strength of monaural
excitation, and had M/B ratios that ranged from 0.0-0.77
(mean 0.38, Fig. 14C). Monaural responsiveness of the ear
on the preferred side was available for 30 LF cells, and for
24/ 30, monaural responsiveness of the other ear was also
available. If monaural stimulation of each ear was excitatory, the higher value was used for the M/B ratio. Most
cells (83%, 20/24) for which responsiveness of both ears
was available exhibited greater responsiveness to stimul;ition of the ear on the preferred side, and for the remainder
the opposite was true (e.g., Fig. 12).
Monaural and binaural thresholds
For most cells, thresholds to monaural and binaural
noise stimulation were available from ALRA data sets (see
legend of Fig. 15 ) and are compared in a scatterplot (Fig.
15A). Monaural thresholds for the ear on the preferred side
BINAURAL
90
DIRECTIONAL
I
2207
CELLS IN AI
I
-c
CONTRA
PLUG
n
.
.
.
.
18936-16
-90
.
I
-60
IPSI
-30
AZIMUTH
0
30
(DEGREES)
60
90
-90
-60
-30
AZIMUTH
IPSI
CONTRA
0
30
(DEGREES)
90
C
70
-90
-60
IPSI
-30
AZIMUTH
0
30
(DEGREES)
E
60
- -
NPI
NP2
-
NP3
0.0
-10
90
AT
10
30
CONTRA
50
SPL
60
9
CONTRA
0”
AZIMUTH
70
90
(dB)
0.4
-
NPl
NP2
--
0.0
-90
NP3
-60
IPSI
-30
AZIMUTH
0
30
(DEGREES)
60
90
CONTRA
FIG. 10. An M-type LF cell with lower thresholds to binaural than to monaural stimulation (8936-16; BF, 10 kHz).
A-C: ALRAs obtained using the treatment condition shown in top left corner. Maximum responses were 0.55, 0.10, and
0.15 spikes/stimulus, respectively; 20 stimulus repetitions. D: level functions at maximal azimuth (0’ ). E: azimuth functions. Separate ANOVAs were used to test the effects of ipsi- and contralateral plugging. The overall effect of plugging each
ear was significant (contralateral: &- = 0.000 1, PTA== 0.24, PTA= 0.000 1, and PTL= 0.000 1; ipsilateral: PT= 0.0001, PTAL=
0.08, PTA= 0.0001, and PTL= 0.06). Post hoc tests on the data combined across levels revealed binaural facilitation
(corrected CY= 0.05 /7 = 0.007). Binaural responses were significantly larger than ipsi- or contralateral plug responses at
-30’ to 90*. Post hoc tests on data for individual azimuth-level combinations (corrected cy = 0.05/28 = 0.00 18) showed
significant differences between binaural and monaural responses for each ear at O*, 40 dB and 0°, 60 dB (circled plus signs on
A and D) ; between binaural and ipsilateral monaural responses at 90”, 60 dB; and between binaural and contralateral
monaural responses at 60”, 60 dB and 90”, 80 dB.
were similar to binaural thresholds in EI cells (Fig. 15A,
also see ALRAs in Figs. 1-4). Of the 19 EI cells for which
thresholds were available, 18 showed differences ~5 dB.
The average threshold difference for monaural and binaural stimulation was 1.O dB and was not statistically significant.
Many midline cells were unresponsive to monaural stimulation at the preferred azimuths, and thus monaural
thresholds could not be determined (“U” in Fig. 15A). The
remaining cells had monaural thresholds that were 15-39
dB higher than the binaural thresholds.
Thresholds were available for 28 LF cells. Monaural
thresholds were available for the ear on the preferred side of
all 28 cells, and were also available for the other ear in
2 1/ 28 cells. If monaural stimulation of each ear was excitatory, the lowest threshold of the two was plotted. In most
cases ( 18 / 2 1 ), the ear on the preferred side had the lowest
threshold and also gave the strongest monaural response.
The strongest response for the remaining cells was produced by the ear on the nonpreferred side. For one of these,
thresholds were also lowest on the nonpreferred side and for
the other two, thresholds for the two ears were equal. Monaural/binaural threshold differences of 4 dB (e.g., Figs. 8
and 9) were exhibited by 39% ( 11/28) of the LF sample. Of
the remaining 17 cells, 2 were completely unresponsive to
monaural stimulation (i.e., Fig. 7) and 15 had monaural
2208
F. K. SAMSON,
P. BARONE,
J. C. CLAREY,
,
-in!
-,“I
-90
40
IPSI
C
-30
AZIMUTH
0
1
3‘0
I
6-O
90
t
.I90
-60
1.5
-
NPI
-
NP2
-30
AZIMUTH
IPSI
CONTRA
(DEGREES)
AND T. J. IMIG
-
AT
-30”
0
(DEGREES)
30
60
4 0
CONTRA
AZIMUTH
. . . . . .*...-.
NPl
CP
11.1..*.....
IP
NP2
-
0.0
-90
IPSI
-60
-30
AZIMUTH
0
30
60
(DEGREES)
90
0.0
-10
10
30
SPL
CONTRA
50
(dB)
70
90
FIG. 11. An M-type LF cell with lower thresholds to binaural than to monaural stimulation (902 1- 10; BFs, 5 and 8
kHz). A and B: ALRAs obtained under binaural and contralateral plug conditions. Maximum responses were 2.3 and 2.0
spikes/stimulus, respectively; 10 stimulus repetitions. The cell was unresponsive with the ipsilateral ear plugged. C: azimuth
functions. D: level functions at maximal (-30”) azimuth. An ANOVA revealed significant azimuth-dependent and leveldependent ear plugging effects (PT= 0.15, PTA== 0.003, PTL= 0.022, PTA= 0.00 1). Post hoc tests on the data combined
across levels (corrected cy= 0.05 / 7 = 0.007 ) revealed that binaural responses were significantly larger than contralateral plug
responses on the ipsilateral side and significantly smaller than contralateral plug responses on the contralateral side. Post hoc
tests on data for individual azimuth-level combinations (corrected cy= 0.05 / 28 = 0.00 18) revealed azimuth-level combinations at which binaural responses were significantly smaller ( circled minus signs, A ) and significantly larger (circled plus
signs, A and D) than contralateral ear plug responses.
thresholds that were between 6 and 56 dB higher than binaural thresholds. Monaural thresholds averaged 27.1 dB
higher than binaural thresholds for the combined sample of
midline and LF cells, and the difference was statistically
significant.
EI and LF cells exhibit diferent ALRA architectures
The orientation of iso-response contour lines in the preferred quadrant of EI and LF cell binaural ALRAs showed
systematic differences. The orientation in EI (Figs. 1-3 )
and some LF (Fig. 8 and 9) cells paralleled excitatory
thresholds to monaural stimulation of the ear on the preferred side showing that suprathreshold response magnitude was a function of monaural excitatory threshold. In
contrast, contours were oriented obliquely in many LF cells
and sloped from minimum levels at or near the midline to
higher levels toward the lateral pole (Figs. 11A, 12A, and
13, A and D) . The contours did not parallel monaural excitatory thresholds, and this pattern differed from most EI
cells for which contours exhibited shallower slopes and did
not reach minima at the midline.
DISCUSSION
Two classes of high-BF, azimuth-sensitive neurons can
be distinguished in AI on the basis of their responses to
unilateral ear plugging. One class, described in this report,
consisted of cells whose azimuth tuning depended entirely
upon binaural stimulation (BD cells). Their responses
under unilateral ear plug conditions were characterized by
insensitivity to azimuth or, in a few cases, by striking
changes in the location of the response peak in the azimuth
function. This discussion compares patterns of monaural
and binaural responses to noise bursts presented in the free
field with patterns of responses to ILDs present in tone
bursts
*
El mechanisms
EI neurons in AI of the cat (Brugge et al. 1969; Phillips
and Irvine 198 1, 1983; Reale and Kettner 1986; Semple
and Kitzes 1993a; reviewed in Clarey et al. 1992) and other
species ( Brugge and Merzenich 197 3; Kelly and Sally 19 8 8 )
are sensitive to interaural level differences (ILDs) present
in high-frequency tone bursts. These cells cease to respond
when level at the inhibitory ear exceeds that at the excitatory ear. Consequently, it has been suggested that EI cells
should respond selectively to sound sources on the side of
the excitatory ear. Our results are consistent with such predictions, even though they were obtained using noise stimulation.
Unilateral plugging of the inhibitory ear revealed that EI
BINAURAL
A
is
m
DIRECTIONAL
2209
CELLS IN AI
90
70
50
ti!
cn 30
-10
-90
-60
IPSI
-30
AZIMUTH
0
30
60
(DEGREES)
90
-
0
-60
-30
IPSI
CONTRA
. . . . .. 0.. . .
-90
-60
IPSI
-30
AZIMUTH
0
30
60
(DEGREES)
E
90
0
AZIMUTH
-10
AT
NPI
CP
30
IO
CONTRA
. . . . . .0 . . . .
---h-e
0
0”
90
CONTRA
AZIMUTH
70
90
(cm)
NPl
CP
IP
NP2
-
---__
60
50
SPL
0.6
30
(DEGREES)
0
&
e-
*---
CLH-
0
0
..Q”‘----
..--
I
90
IPSI
1
-60
..---
-O..*
l
.
..--
I
-30
AZIMUTH
I
I
I
0
30
(DEGREES)
I
60
90
CONTRA
12. A bilaterally excited, M-type LF cell ( 902 l-09; BF, 8 kHz). A-C: ALRAs obtained under different treatment
conditions. Maximum responses were 1.O, 0.3, and 0.8 spikes/ stimulus, respectively; 10 stimulus repetitions. D: level
functions obtained at maximal azimuth. E: azimuth functions. Separate ANOVAs were used to test the effects of ipsi- and
contralateral plugging. There was a significant overall effect of plugging the contralateral ear ( PT = 0.000 1, PTAL = 0.18,
P, = 0.0009, and P, = 0.14). Post hoc tests on the data combined across levels (corrected a! = 0.05 / 7 = 0.007) revealed
that binaural responses were significantly greater than contralateral plug responses at 0’) -3O”, and -60’ (circled plus signs,
E). Post hoc tests on data for individual azimuth-level combinations (corrected cy = 0.05/28 = 0.00 18) failed to show
significant differences. The ANOVA showed a significant azimuth-dependent effect for ipsilateral ear plugging ( PT = 0.12,
P TAL= 0.33, PTA = 0.0001, and PTL = 0.32). Post hoc tests on the data combined across levels (corrected CY= 0.05 /7 = 0.007)
revealed that binaural responses were significantly larger at 0’ and -30' (circled plus signs, E) and significantly smaller
(circled minus sign) than ipsilateral plug responses at 60’. Post hoc tests on data for individual azimuth-level combinations
(corrected CY= 0.05 / 28 = 0.00 18) failed to show significant differences.
FIG.
cells utilized two different mechanisms of azimuth tuning.
The azimuth tuning of BD-EI cells, described in this report,
depended upon binaural stimulation, as they responded
nonselectively to azimuth with the inhibitory ear plugged.
In contrast, the azimuth tuning of most MD cells depended
in part upon binaural inhibition and in part upon monaural
spectral cues at the excitatory ear (MD-E1 cells) ( Samson et
al. 1993). Binaural inhibition had a similar effect on the
azimuth tuning of both types of EI cells, it suppressed responses to directions on the side of the inhibitory ear.
A relatively small proportion of the sample of BD-EI cells
exhibited azimuth tuning that was relatively independent
of stimulus level over a range of 20-60 dB. EI cells with
level-tolerant ILD sensitivity have been described in the
lateral superior olive (LSO) (Boudreau and Tsuchitani
1968), the dorsal nucleus of the lateral lemniscus (DNLL)
(Brugge et al. 1970), the inferior colliculus (IC) (Irvine and
Gago 1990), the medial geniculate body (MGB) ( Ivarsson
et al. 1988), and AI (Brugge et al. 1969) of the cat’s auditory system. Such cells also have been found in the deep
layers of the superior colliculus (SC) using dichotically presented noise and tonal stimulation (Hirsch et al. 1985; Wise
2210
F. K. SAMSON,
P. BARONE,
J. C. CLAREY,
AND
T. J. IMIG
90
A
0
70
0
8
m
.
-90
-60
-30
IPSI
-90
0
AZIMUTH
-60
-30
0
AZIMUTH
IPSI
30
60
(DEGREES)
30
60
(DEGREES)
10
30
SPL
50
(dB)
-90
-60
IPSI
90
-90
-30
AZIMUTH
-60
IPSI
CONTRA
NPI
IP
-
NPl
---..+.--.-
CP
NP2
-
NP2
70
90
0
30
60
0
30
90
60
(DEGREES)
CONTRA
AT
SPL
90
CONTRA
(DEGREES)
-30
AZIMUTH
---&--.
-
-10
90
CONTRA
l
30”
AZIMUTH
(dB)
FIG. 13. Two LF cells with NM-type level tuning that depended upon binaural stimulation. A and B: ALRAs of unit
8942-07 (BF, 17 kHz) obtained under binaural and ipsilateral plug conditions. Maximum
responses were 1.6 and 1.05
spikes/stimulus,
respectively; 20 stimulus repetitions. The cell was unresponsive with the contralateral ear plugged. An
ANOVA showed significant azimuth- and level-dependent effects of ipsilateral ear plugging (P, = 0.97, PTA== 0.000 1, PTA=
0.000 1, and PTL = 0.000 1) . Post hoc tests on the data combined across levels (corrected a! = 0.05 /7 = 0.007) revealed that
binaural responses were significantly smaller than ipsilateral plug responses at -9O”, -6O”, and -30’ and significantly larger
than ipsilateral plug responses at 0’) 60”, and 90°. Post hoc tests on data for individual azimuth-level combinations
(corrected CY= 0.05 /28 = 0.00 18 ) failed to show significant differences. C: level functions at maximal (0’ ) azimuth for unit
8942-07. D and E: ALRAs of unit 8942- 12 (BF, 17 kHz) obtained under binaural and ipsilateral plug conditions. Maximum responses were 1.4 and 1.1 spikes/stimulus,
respectively; 20 stimulus repetitions. F: level functions at maximal ( 30° )
azimuth for unit 8942- 12. An ANOVA revealed a significant overall effect of plugging the ipsilateral ear ( PT = 0.000 1) and
all interaction terms were also significant ( PTAL= 0.01, PTA = 0.0001, and PTL = 0.000 1 ), indicating that the effect of ear
plugging depended on azimuth and level. Post hoc tests on the data combined across levels (corrected a! = 0.05 /7 = 0.007)
revealed that binaural responses were significantly smaller than ipsilateral plug responses at -9O”, -6O”, -3O”, and O” and
significantly larger than ipsilateral plug responses at 30°. Post hoc tests on data for individual azimuth-level combinations
(corrected cx = 0.05/28 = 0.00 18 ) revealed azimuth-level combinations at which binaural responses were significantly
smaller (circled minus signs) and larger (circled plus sign) than ipsilateral plug responses (D and F).
and Irvine 1985 ) . The balance of excitation and inhibition
that is maintained over a wide range of levels in these cells
stands in striking contrast to inhibitory domination that
occurs with increasing level in other EI cells (Figs. 3 and 4).
Although the LSO is an initial site of EI response synthesis in the ascending auditory pathway, it is uncertain to
what extent level-tolerant EI cells at higher levels of the
auditory pathway might reflect binaural processing in the
LSO. There are other sites of excitatory/inhibitory
convergence besides the LSO (Glenn and Kelly 1992; Sally and
Kelly 1992)) as shown by the finding of EI cells in the inferior colliculus after bilateral destruction of the LSO (Li and
Kelly 1992). Iontophoresis of the y-aminobutyric acid
(GABA) antagonist bicuculline blocks inhibitory input to
some EI cells in the IC suggesting that excitatory/inhibitory
convergence takes place in the IC (Park and Pollak 1993 ) .
BINAURAL
A
DIRECTIONAL
CELLS
IN AI
2211
8
go-
,
u
m
3
LIMA
.
,a* 0’ ’ d
,’
.’
,*’
,’
a’ ,*’
,,’
*
.
A
70.
l
50-
.
,’
.’
A
’
,~i~/
.’ . a’
A% ,’
.’
*a’0 ,,’
I.
ko
CELLS
*
a’
-10
!.(
b
12
%
E;
10
30
n=30
?I
2
(n=9)
50
70
THRESHOLD
(dB
SPL)
20
6
LF CELLS
El (n=l9)
MIDLINE
LF (n=26)
l
BINAURAL
B
,’
BD CELLS
0
A
. ,/p
n=9
,a’
,0’
*’
.
1 oMIDLINE
,’
t . ,*’ ,’
,’ ,a’
.
33 o0 _-
,’
,’
10
a*’
,‘A
a
,,a;
0
,’
.’
a’
,-
l
,.’
,-
**’
,**”
0
,’
#’
80’
A&+
1
P
0
A
A
O
0
,*‘A
.’
,’
,A#‘*0
2
5
,’ l ’ 0
a’
*’
#’
l’
0
A
l
BD-El
MD-El
MD-E0
(n=l9)
(n=17)
(n=6)
-10
!.C
MI0
RATIO
RG.
14. Ratio of monaural to binaural responsiveness for facilitatory
cells. Monaural and binaural responsiveness was measured at preferred
azimuths, i.e., the locations where binaural azimuth function values were
275% of maximum. Responsiveness at each preferred azimuth was the
value of the azimuth function in spikes/stimulus,
and these values were
averaged over preferred azimuths if there was more than one. This gave an
estimate of responsiveness for each binaural and monaural ALRA data set.
Responsiveness was averaged over repeated ALRA data sets, if repetitions
were available. In the case of cells that received bilateral monaural excitation, the strongest monaural response was used to compute the monaural
to binaural responsiveness (M/B) ratio. A: M/B ratios for EI cells. B:
M/B ratios for midline cells. C: M/B ratios for LF cells.
A majority of EI cells in our sample, including both BD
and MD types, received strongly nonmonotonic input from
the excitatory ear. Using dichotic tonal stimulation, Semple
and Kitzes ( 1993a) described EI cells in AI whose nonmonotonic level tuning reflected nonmonotonic monaural
excitatory input. Although nonmonotonic excitatory input
is a common feature of cortical EI cells, it appears to be less
common at lower levels of the auditory system. Nonmonotonic excitatory input is uncommon in EI cells in the LSO
-10
0
10
20
30
BINAURAL
THRESHOLD
(dB SPL)
RG.
15. Comparison of thresholds to binaural and monaural noise
stimulation.
Thresholds [sound-pressure levels ( SPLs) corresponding to
the 5% iso-response contour] were averaged over preferred azimuths (binaural azimuth function values > 75%) to provide an estimate of threshold
for each ALRA data set. Thresholds were averaged over repeated ALRA
data sets, if repetitions were available. Diagonal lines indicate a5 dB differences. A: thresholds to binaural and monaural noise stimulation for 3
groups of BD cells. The letter “U” on the y-axis indicates cells (LF, 2;
MIDLINE,
6) that were unresponsive to monaural stimulation. B: thresholds to binaural and monaural noise stimulation for binaural directional
(BD)-EI, monaural directional (MD)-EI, and MD-E0 cells. A monaural
threshold of SO-dB SPL was assigned to monaurally unresponsive cells in
order to include them in the statistical analysis. A two-factor ANOVA on
thresholds of the different cell groups revealed an overall significant difference between binaural and monaural thresholds (P < 0.0004)) an overall
significant difference of thresholds between cell groups (P < 0.000 1 ), and a
significant interaction term (P < 0.000 1)) indicating that the effect of ear
plugging on thresholds was different for different cell groups. A t test
showed that the means for monaural and binaural thresholds in BD-EI and
MD (EO and EI) cells were not significantly different (BD-EI, mean difference 0.95 dB, P = 0.19; MD, mean difference 0.09 dB, P = 0.89). The
combined sample of midline and LF cells had monaural thresholds that
were significantly higher than binaural thresholds (mean difference 27.14
dB, P = 0.0001).
2212
F. K. SAMSON,
P. BARONE,
(Boudreau and Tsuchitani 1970) or in the DNLL (Brugge
et al. 1970), although in this latter case, relatively few cells
have been studied. EI cells that receive nonmonotonic excitatory input are present in the cat’s IC but in smaller proportion than in AI (e.g., Irvine and Gago 1990).
There remains an element of uncertainty in our classification of EI cells because most ( 17/ 2 1) were classified on the
basis of plugging only one ear. This was sufficient to determine that one ear was excitatory and the other was inhibitory. A minority ( 5 / 22) of cells that exhibited binaural inhibition was studied with unilateral plugging of each ear, and
for four, only one of the two ears was found to be excitatory.
However, one cell received excitatory input from both ears,
and thus the cell was classified as EE / I. In the present study,
one out of five cells that would have been classified as EI on
the basis of plugging a single ear actually turned out to be an
EE/I cell. This finding suggests that 20% of the EI sample
(so classified on the basis of plugging only one ear) might in
fact be EE/ I cells. Samson et al. ( 1993) studied 14 MD cells
with unilateral plugging of each ear. All would have been
classified as EI on the basis of plugging only the ear on the
nonpreferred side, but one turned out to be an EE/I cell.
This suggests that -7% of the MD cells classified as EI on
the basis of plugging a single ear might actually be EE/ I
cells. Cells with EE/I properties have previously been
reported in dichotic studies in AI of the cat (Phillips and
Irvine 1983; Semple and Kitzes 1993a), but previous dichotic studies suggest that they are relatively uncommon
(Imig and Adrian 1977; Imig and Brugge 1978; Imig and
Reale 198 1; Middlebrooks and Zook 1983; Middlebrooks
et al. 1980). They also have been reported in the IC of the
bat (Fuzessery et al. 1990).
Midline cells
J. C. CLAREY,
AND
T. J. IMIG
Some midline cells exhibited high-threshold responses on
the side of the plugged ear, and such responses also may be
explained by selectivity to zero ILD. Midline stimulation
produces zero ILD under binaural conditions, but with one
ear plugged, level at the TM of the unplugged ear will exceed that at the plugged ear resulting in a nonzero ILD.
Under unilateral ear plug conditions, ILD magnitude
would be expected to reach a minimum at sound directions
on the side of the plugged ear because the sound shadow
produced by the head and the pinna reduce the level at the
unplugged ear thus bringing it closer to the level at the TM
of the plugged ear. If ILD is reduced sufficiently, the cell
will respond. Higher thresholds would be expected for the
unilateral plug response than the binaural response because
sound reaching each ear would be attenuated either by the
ear plug or by the sound shadow of the head.
Midline-PB cells also are present in the MGB. In the cat,
PB cells selective to zero ILD have been reported using dichotic noise (Ivarsson et al. 1988) and tonal (Aitkin and
Webster 1972) stimulation. Midline cells also have been
identified using free-field noise stimulation with ear plugs
(Irons 1989). In contrast, dichotic (Hind et al. 1963; Irvine
and Gago 1990; Rose et al. 1966) and free-field studies
(Aitkin and Martin 1987; Calford et al. 1986; Moore et al.
1984a,b; Semple et al. 1983) suggest that these rarely are
encountered in the IC or at lower levels of the cat’s auditory
pathway (Brownell et al. 1979; Caird and Klinke 1983;
Guinan et al. 1972; Tsuchitani 1977). This suggeststhat the
MGB is a site of synthesis of PB responses, but there may be
other sites as well. PB and midline cells have been described
in the cat’s SC using dichotic noise stimulation (Wise and
Irvine 1983, 1984), dichotic tonal stimulation (Hirsch et
al. 1985 ) , and free-field noise stimulation with ear plugs
(Middlebrooks 1987). Because the SC does not receive input from the MGB, this may represent an independent site
of synthesis. Additionally, Kitzes and Dohery ( 1994) have
shown that PB responses may be synthesized in AI by the
convergence of thalamic and callosal inputs. Other species
may exhibit different organizations, as PB cells are present
in the IC of bats (Fuzessery et al. 1990) and kangaroo rats
(Stillman 1972) in small numbers.
Ear plugging demonstrated facilitation in midline-PB
cells, however under other conditions, binaural inhibition
may be seen. Midline cells in the cat’s MGB, studied under
nitrous oxide anesthesia, are excited at zero ILD, and their
spontaneous activity is inhibited at nonzero ILDs (Ivarsson
et al. 1988). In our study, binaural inhibition was defined
by an excitatory response that was larger under monaural
than binaural conditions. Because midline cells were unresponsive to monaural stimulation, and were not spontaneously active, there could, by definition, be no demonstration of binaural inhibition.
Midline cells were selective for locations near the midline, and they either failed to respond to any sound direction or responded weakly with either ear plugged. Midline
cells appear functionally identical to the PB cells in AI described using dichotic tonal stimulation (Hall and Goldstein 1968; Kitzes et al. 1980; Phillips and Irvine 198 1,
1983; Semple and Kitzes 1993b). PB cells responded maximally to zero ILD (corresponding to the midline) and either failed to respond or responded poorly to monaural
stimulation.
In addition to low-threshold responses that occurred at
the midline, some midline cells exhibited high-threshold
responses at lateral azimuths (e.g., Fig. 5). Sensitivity to
zero ILD, which accounts for midline preference, also may
account for these lateral responses. For many frequencies,
ILDs are a nonmonotonic function of azimuth, increasing
from zero at the midline to a maximum within a lateral
frontal quadrant and then decreasing towards the lateral
pole (Irvine 1987 ) . If the magnitude of the ILD at the lat- LF cells
eral pole is sufficiently reduced, then cells selective for zero
ILD might be expected to respond to sound directions near LF cells comprise a diverse group of neurons, and by definithe lateral pole. The higher threshold of the lateral compo- tion all had lateral azimuth preferences. Most received excitatory input from one or both ears, with the ear on the prenent of the cell’s response is consistent with the observation
that acoustic gain is greater at the midline than at the lateral ferred side usually providing the strongest monaural input.
Commonly, LF cells exhibited binaural facilitation on the
poles.
BINAURAL
DIRECTIONAL
side of the ear that produced the greatest excitatory input
and exhibited binaural inhibition on the other side. Neurons with corresponding response patterns to tonal dichotic
stimulation, i.e., exhibit binaural facilitation for ILDs that
favor the excitatory ear and binaural inhibition for ILDs
that favor the other ear, have been described in AI (Phillips
and Irvine 198 1; Reale and Kettner 1986; Semple and
Kitzes 1993a,b), the MGB (Aitkin and Dunlop 1968), and
the IC (Benevento et al. 1970; Irvine and Gago 1990) of the
cat’s auditory system. The existence of mixed interactions
in the cat’s MGB also has been documented using free-field
noise stimulation and ear plugging (Irons 1989). In other
species, facilitatory and mixed interactions also have been
demonstrated in AI (chinchilla: Benson and Teas 1976; rat:
Kelly and Sally 1988 ) and in the IC (kangaroo rat: Stillman
1972; gerbil: Semple and Kitzes 1987; bat: Fuzessery et al.
1990; Park and Pollak 1993) using tonal, dichotic stimulation. Outside of the lemniscal auditory system, nonzero
ILD selective (Hirsch et al. 1985; Wise and Irvine 1984,
1985) and azimuth-sensitive (Middlebrooks 1987) LF cells
showing mixed interactions have been described in the SC
of the cat.
Park and Pollack ( 1993) have demonstrated that binaural facilitation is abolished in many ILD sensitive neurons in the bat’s IC by iontophoresis of bicuculline, a
GABA-receptor antagonist. This suggeststhat binaural facilitation in many cells is a product of disinhibition that occurs in the IC. Nevertheless, there appear to be other sites of
synthesis of facilitatory interactions as discussed above for
midline-PB cells.
A few LF cells were unresponsive or poorly responsive
under unilateral plug conditions, similar to midline-PB
cells. If studied using dichotic stimulation, these cells presumably would exhibit nonzero ILD selectivity. To our
knowledge there are no previous reports of cells with lateral
azimuth (or nonzero ILD) preferences that do not respond
to monaural stimulation.
CELLS
IN AI
2213
are consistent with such a mechanism. First, facilitation
was replaced by inhibition at high levels in some TWINS
(Semple and Kitzes 1993b), as is the case in some NM-type
facilitatory cells (Fig. 13). Second, TWINS and NM facilitatory cells exhibit similar patterns of monaural responses.
Some TWINS, which responded maximally to 0 ILD, were
unresponsive or poorly responsive to monaural stimulation
(Semple and Kitzes 1993b), and these correspond to NMtype midline cells (Fig. 6). Other TWINS responded only to
contralateral or ipsilateral stimulation, or to monaural stimulation of either ear, and monaural responses could be either monotonic or nonmonotonic as was the case for most
NM-type LF cells (e.g., Fig. 13). Third, TWINS were most
responsive to ILDs favoring the ear that provided the
greater amount of excitatory input. Correspondingly, the
maximal response of NM-type LF cells usually occurred on
the side of the ear producing the greater amount of excitatory input (Fig. 13).
It was not uncommon for NM-type LF cells to exhibit
multipeaked responses, with one peak located at or near the
midline and another near the lateral pole of the preferred
side (e.g., Fig. 13). Multipeaked responses occurred to
noise and, in one case, to tones (not illustrated), suggesting
that they did not necessarily reflect sensitivity to spectral
cues. Cells exhibiting TWIN tuning might be expected to
exhibit multipeaked responses. This is because they respond maximally to a single ILD (corresponding to the best
binaural combination) and submaximally at other ILDs.
At most frequencies in the BF range of our sample, ILDs
are a nonmonotonic function of azimuth, increasing from
zero at the midline to a maximum within a lateral frontal
quadrant and then decreasing towards the lateral pole (Irvine 1987). If the best binaural combination corresponds
to a submaximal ILD, then there should be two (or possibly
more) locations within a frontal quadrant corresponding
with the best binaural combination.
Mechanisms of azimuth sensitivity
Bilateral nonmonotonic facilitation
Bilateral nonmonotonic facilitation is seen in some highBF neurons in cat AI (Semple and Kitzes 1993b). Neurons
displaying this type of interaction have been referred to as
TWINS because they exhibited nonmonotonic tuning to
both average binaural level (average of the levels delivered
to each ear) and ILDs. TWINS were initially described in
the gerbil’s IC ( Semple and Kitzes 1987 ), although they are
less common there than in cat AI (Semple and Kitzes
1993b). Binaural facilitation in TWINS is a nonmonotonic
function of level at each ear, and there is an optimal SPL at
each ear (the best binaural combination) for which binaural facilitation is maximal (Semple and Kitzes 1993b).
Increases or decreases from the optimal SPL at either ear
cause a decrease in the neuron’s responsiveness.
A model based on bilateral nonmonotonic facilitation
and consistent with TWIN tuning can mimic some characteristics of NM-type facilitatory cells (including those with
midline and lateral azimuth preferences), i.e., selectivity
for restricted ranges of level and azimuth (Imig et al. 1990).
Some NM-type facilitatory cells have characteristics that
The effect of ear plugging provides evidence for two
classes of high-frequency AI neurons that utilize different
mechanisms of azimuth sensitivity. The azimuth sensitivity
of BD cells, described in this report, appears to have substantial dependence upon ILDs present in noise. Dichotic
studies have revealed the existence of AI neurons that are
sensitive to ILDs present in tonal stimuli. If azimuth tuning
is derived from ILD sensitivity, then these studies predict
certain expected relationships between azimuth tuning,
monaural inputs, and binaural interactions. The responses
of BD cells are largely consistent with these predictions suggesting that they derive azimuth tuning from ILDs present
in noise stimuli. Mechanisms by which neurons integrate
the noise spectrum to extract ILDs are unknown, although
ITD tuning of low-frequency IC neurons to noise stimulation is closely approximated by the linear summation of
ITD tuning at individual frequencies (Chan et al. 1987; Yin
et al. 1986). In contrast to BD cells, the azimuth sensitivity
of MD cells is derived from monaural cues that are present
in noise (Samson et al. 1993). In response to monaural
tone bursts, MD cells lack azimuth sensitivity, suggesting
2214
F. K. SAMSON,
P. BARONE,
that the cells derive azimuth sensitivity from monaural
spectral cues that are present in noise but not tones.
Sensitivity to MD cues has been documented in neurons
receiving strictly monaural input, as well as cells receiving
EI input (Samson et al. 1993), but there is little evidence
for such sensitivity in cells exhibiting binaural facilitation.
Only one cell in a sample of 27 MD cells appeared to show
binaural facilitation. As this was not confirmed by repeated
testing, it could have been the result of uncontrolled variation in responsiveness that just happened to coincide with
ear plugging (Samson et al. 1993). Sensitivity to MD cues
was not evident in the monaural responses of any of the
cells in our sample of BD facilitatory cells. Nevertheless,
this does not mean that binaural facilitatory cells necessarily lack sensitivity to MD cues. It is possible that MD cues
could play a role in direction specific expression of binaural
interactions in some cells of this group.
Level tuning
Monaural stimulation of the ear on the preferred side can
account for the binaural level tuning at preferred azimuths
of many azimuth-sensitive cells. The vast majority of BDEI cells exhibited similar thresholds to monaural and binaural stimulation, as was the case for MD-E1 and MD-E0
cells (Fig. 15B). Furthermore the responses at suprathreshold levels of a majority of BD-EI cells and all MD cells
( Samson et al. 1993) were unaffected by plugging the inhibitory ear. Binaural inhibition can account for decreased responsiveness at high levels of noise stimulation in a minority of EI cells, as is the case for tonal response of some EI
cells (Semple and Kitzes 1993a).
Relatively few LF cells had monaural level functions that
were similar to binaural level functions, both in terms of
threshold and function shape. It was much more common
for facilitatory cells to exhibit different patterns of monaural and binaural level tuning. All midline cells and some
LF cells responded poorly, if at all, to monaural stimulation, so their binaural and monaural level tuning were not
comparable. A majority of the LF sample exhibited lower
thresholds to binaural than monaural stimulation. LF cells,
including those with similar monaural and binaural thresholds, often exhibited different shapes of level functions to
binaural and monaural stimulation. Binaural level function
shape reflected level-dependent patterns of binaural interactions. Cells with NM-type level functions usually exhibited binaural facilitation at low levels and no facilitation or
inhibition at high levels. Cells with M-type level functions
exhibited facilitation over most or all of the range of levels
to which they responded, although the level range over
which facilitation was strongest varied among cells. Previous dichotic studies in AI using tonal stimulation have
described level-dependent differences in strength of facilitation in NM-type mixed interaction neurons (cat: Reale and
Kettner 1986; Semple and Kitzes 1993b, rat: Kelly and
Sally 1988), but not in M-types.
Most neurons with nonmonotonic level tuning are azimuth sensitive (Imig et al. 1990), showing that nonmonotonicity and directional tuning are linked together. Although the functional significance of this linkage is not
J. C. CLAREY,
AND
T. J. IMIG
known, ear plugging shows that nonmonotonic level tuning
results from at least three different mechanisms. Nonmonotonic monaural excitatory input accounts for binaural nonmonotonic responses in MD-E1 and MD-E0 cells, in a majority of BD-EI cells, and in a few LF cells. Binaural inhibition contributes to nonmonotonicity
in a minority of
BD-EI cells. Level-dependent facilitation and inhibition
produce nonmonotonic responses in midline and LF cells.
Lateralized azimuth tuning is characteristic of both EI
and LF cells, although there are differences in ALRA architecture. The orientation of iso-response contours in many
EI cells generally paralleled excitatory ear thresholds showing that orientation reflected direction-dependent gain at
the excitatory ear. In contrast, iso-response contours in the
preferred quadrant of some LF cells coursed obliquely from
low levels near the midline to higher levels at the lateral pole
and do not seem to reflect directional gain at the ear on the
preferred side. It was suggested previously that such an orientation may be a consequence of the effect of direction
dependent gain at each TM and binaural facilitation (Imig
et al. 1990). The finding that obliquely oriented iso-response contours are a characteristic of facilitator-y cells and
not EI cells seems to support this idea.
C. Bailey carefully prepared histological materials and graphics, D. Billheimer provided advice on statistics, and H. Cheng provided computer
programming. Critical reviews by Dr. D. R. F. Irvine and another anonymous reviewer were very helpful.
This work was supported by the National Institute on Deafness and
Other Communicative
Disorders Grant DC-001 73 and BRSG SO7 RR05373 and 554855 awarded by the Biomedical Research Support Grant
Program, Division of Research Resources, National Institutes of Health.
Present addresses: P. Barone, Cerveau et Vision, INSERM Unite 37 1, 18
Avenue du Doyen L&pine, 69500 BRON, France; J. C. Clarey, Vision,
Touch, and Hearing Research Centre, Dept. of Physiology and Pharmacology, University of Queensland, Queensland 4072, Australia.
Address reprint requests to T. J. Imig.
Received 7 September 1993; accepted in final form 17 February 1994.
REFERENCES
AITKIN, L. M. AND DUNLOP, C. W. Interplay of excitation and inhibition
in the cat medial geniculate body. J. Neurophysiol. 3 1: 44-6 1, 1968.
AITKIN, L. M. AND MARTIN, R. L. The representation of stimulus azimuth
by high best-frequency azimuth-selective neurons in the central nucleus
of the inferior colliculus of the cat. J. Neurophysiol.
57: 1185-1200,
1987.
AITIUN, L. M. AND WEBSTER, W. R. Medial geniculate body of the cat:
organization and responses to tonal stimuli of neurons in ventral division. J. Neurophysiol. 35: 365-380, 1972.
BARRETT, T. W. The response of auditory cortex neurons in cat to various
parameters of acoustical stimulation. Brain Rex 28: 579-58 1, 197 1.
BENEVENTO, L. A., COLEMAN, P. D., AND LOE, P. R. Responses of single
cells in cat inferior colliculus to binaural click stimuli: combinations of
intensity levels, time differences, and intensity differences. Brain Res.
17: 387-405, 1970.
BENSON, D. A., HIENZ, R. D., AND GOLDSTEIN, M. H. Single-unit activity
in the auditory cortex of monkeys actively localizing sound sources:
spatial tuning and behavioral dependency. Brain Res. 2 19: 249-267,
1981.
BENSON, D. A. AND TEAS, D. C. Single-unit study of binaural interaction
in the auditory cortex of the chinchilla. Brain Res. 103: 3 13-338, 1976.
BEYER, W. H. CRC Handbook of Tables for Probability and Statistics.
(2nd ed.), Boca Raton, Florida: CRC Press, 1968.
BOUDREAU, J. C. AND TSUCHITANI, C. Binaural interaction in the cat
superior olive S segment. J. Neurophysiol. 3 1: 442-454, 1968.
BOUDREAU, J. C. AND TSUCHITANI, C. Cat superior olive S-segment cell
BINAURAL
DIRECTIONAL
discharge to tonal stimulation. In: Contributions to Sensory Physiology,
edited by W. D. Neff, New York: Academic, 1970, vol. 4, p. 144-2 13.
BROWNELL, W. E., MANIS, P. B., AND RITZ, L. A. Ipsilateral inhibitory
responses in the cat lateral superior olive. Brain Res. 177: 189-193,
1979.
BRUGGE, J. F., ANDERSON, D. J., AND AITIUN, L. M. Responses of neurons in the dorsal nucleus of the lateral lemniscus of cat to binaural tonal
stimulation. J. Neurophysiol. 33: 44 l-458, 1970.
BRUGGE, J. F., DUBROVSKY, N. A., AITIUN, L. M., AND ANDERSON, D. J.
Sensitivity of single neurons in auditory cortex of cat to binaural tonal
stimulation; effects of varying interaural time and intensity. J. Neurophysiol. 32: 1005- 1024, 1969.
BRUGGE, J. F., DUBROVSKY, N., AND ROSE, J. E. Some discharge characteristics of single neurons in cat’s auditory cortex. Science Wash. DC
146: 433-434, 1964.
BRUGGE, J. F. AND MERZENICH, M. M. Responses of neurons in auditory
cortex of the macaque monkey to monaural and binaural stimulation.
J. Neurophysiol. 36: 1138-l 158, 1973.
CAIRD, D. AND KLINKE, R. Processing of binaural stimuli by cat superior
olivary complex neurons. Exp. Brain Res. 52: 385-399, 1983.
CALFORD, M. B., MOORE, D. R., AND HUTCHINGS, M. E. Central and
peripheral contributions to coding of acoustic space by neurons in inferior colliculus of cat. J. Neurophysiol. 55: 587-603, 1986.
CHAN, J. C. K., YIN, T. C. T., AND MUSICANT, A. D. Effects of interaural
time delays of noise stimuli on low-frequency cells in the cat’s inferior
colliculus. II. Responses to band-pass filtered noises. J. Neurophysiol.
58: 543-561, 1987.
CLAREY, J. C., BARONE, P., AND IMIG, T. J. Physiology of thalamus and
cortex. In: The Mammalian
Auditory Pathway: Neurophysiology, edited
by A. N. Popper and R. R. Fay, New York: Springer-Verlag, 1992, p.
232-334.
EISENMAN, L. M. Neural encoding of sound localization: an electrophysiological study in auditory cortex (AI) of the cat using free field stimuli.
Brain Res. 75: 203-2 14, 1974.
EVANS, E. F. Cortical representation. In: Hearing Mechanisms in Vertebrates, edited by A. V. S. de Reuck and J. Knight. London: Churchill,
1968, p. 272-287.
FUZESSERY, Z. M., WENSTRUP, J. J., AND POLLAK, G. D. Determinants of
horizontal sound localization selectivity of binaurally excited neurons in
an isofrequency region of the mustache bat inferior colliculus. J. Neurophysiol. 63: 1128-l 147, 1990.
GLANTZ, S. A. Primer of Biostatistics. ( 2nd ed.), New York: McGraw-Hill,
1987.
GLENN, S. L. AND KELLY, J. B. Kainic acid lesions of the dorsal nucleus of
the lateral lemniscus: effects on binaural evoked responses in rat auditory cortex. J. Neurosci. 12: 3688-3699, 1992.
GUINAN, J. J., GUINAN, S. S., AND NORRIS, B. E. Single auditory units in
the superior olivary complex. I. Responses to sounds and classification
based on physiological properties. Int. J. Neurosci. 4: 10 l- 120, 1972.
HALL II, J. L. AND GOLDSTEIN JR., M. H. Representation of binaural stimuli by single units in primary auditory cortex of unanesthetized cats. J.
Acoust. Sot. Am. 43: 456-46 1, 1968.
HEFFNER, H. E. AND MASTERTON, R. B. Contribution
of auditory cortex
to sound localization in the monkey. J. Neurophysiol. 38: 1340- 1358,
1975.
HIND, J. E., GOLDBERG, J. M., GREENWOOD, D. D., AND ROSE, J. E. Some
discharge characteristics of single neurons in the inferior colliculus of the
cat. II. Timing of the discharges and observations on binaural stimulation. J. Neurophysiol. 26: 32 l-34 1, 1963.
HIRSCH, J. A., CHAN, J. C. K., AND YIN, T. C. T. Responses of neurons in
the cat’s superior colliculus to acoustic stimuli. I. Monaural and binaural response properties. J. Neurophysiol. 53: 726-745, 1985.
IMIG, T. J. AND ADRIAN, H. 0. Binaural columns in the primary field (AI)
of cat auditory cortex. Brain Res. 138: 24 l-257, 1977.
IMIG, T. J. AND BRUGGE, J. F. Sources and terminations of callosal axons
related to binaural and frequency maps in primary auditory cortex of the
cat. J. Comp. Neural. 182: 637-660, 1978.
IMIG, T. J., IRONS, W. A., AND SAMSON, F. R. Single-unit selectivity to
azimuthal direction and sound-pressure level of noise burst in cat highfrequency primary auditory cortex. J. Neurophysiol. 63: 1448-1466,
1990.
IMIG, T. J. AND REALE, R. A. Ipsilateral corticocortical projections related
CELLS
IN AI
2215
to binaural columns in cat primary auditory cortex. J. Comp. Neural.
203: 1-14, 1981.
IRONS, W. A. Directional selectivity of single units in the auditory thalamus
of cats. (PhD dissertation). Kansas City, KS: University of Kansas,
1989.
IRVINE, D. R. F. Interaural intensity differences in the cat: changes in
sound-pressure level at the two ears associated with azimuthal displacements in the frontal horizontal plane. Hear. Res. 26: 267-286, 1987.
IRVINE, D. R. F. AND GAGO, G. Binaural interaction in high-frequency
neurons in inferior colliculus of the cat: effects of variations in soundpressure level on sensitivity to interaural intensity differences. J. Neurophysiol. 63: 570-59 1, 1990.
IVARSSON, C., DE RIBAUPIERRE, Y., AND DE RIBAUPIERRE, F. Influence of
auditory localization cues on neuronal activity in the auditory thalamus
of the cat. J. Neurophysiol. 59: 586-606, 1988.
JENKINS, W. M. AND MASTERTON, R. B. Sound localization: effects of
unilateral lesions in central auditory system. J. Neurophysiol. 47: 9871016, 1982.
JENKINS, W. M. AND MERZENICH, M. M. Role of cat primary auditory
cortex for sound localization behavior. J. Neurophysiol. 52: 8 19-847,
1984.
KAVANAGH, G. L. AND KELLY, J. B. Contribution
of auditory cortex to
sound localization by the ferret. J. Neurophysiol. 57: 1746- 1766, 1987.
KELLY, J. B. AND SALLY, S. L, Organization
of auditory cortex in the
albino rat: binaural response properties. J. Neurophysiol. 59: 17561769, 1988.
KITZES, L. M. AND DOHERTY, D, Influence of callosal activity upon units
in the auditory cortex of ferret (Mustela putorious) . J. Neurophysiol. 7 1:
1740-1751, 1994.
KITZES, L. M., WREGE, K. S., AND CASSADY, J. M. Patterns of responses of
cortical cells to binaural stimulation. J. Comp. Neural. 192: 455-472,
1980.
KLINGON, G. H. AND BONTECOU, D. C. Localization in auditory space.
Neurology 16: 879-886, 1966.
LI, L. AND KELLY, J. B. Binaural responses in rat inferior colliculus following kainic acid lesions of the superior olive: interaural intensity difference functions. Hear. Res. 6 1: 73-85, 1992.
MIDDLEBROOKS, J. C. Binaural mechanisms of spatial tuning in the cat’s
superior colliculus distinguished using monaural occlusion. J. Neurophysiol. 57: 688-701, 1987.
MIDDLEBROOKS, J. C., DYKES, R. N., AND MERZENICH, M. M. Binaural
response-specific bands in primary auditory cortex (AI) of the cat: topographical organization orthogonal to isofrequency contours. Brain Res.
181: 31-48, 1980.
MIDDLEBROOKS, J. C. AND PETTIGREW, J. D. Functional classes of neurons in primary auditory cortex of the cat distinguished by sensitivity to
sound localization. J. Neurosci. 1: 107- 120, 198 1.
MIDDLEBROOKS, J. C. AND ZOOK, J. M. Intrinsic organization of the cat’s
medial geniculate body identified by projections to binaural responsespecific bands in the primary auditory cortex. J. Neurosci. 3: 203-224,
1983.
MOORE, D. R., HUTCHINGS, M. E., ADDISON, P. D., SEMPLE, M. N., AND
AITKIN, L. M. Properties of spatial receptive fields in the central nucleus
of the cat inferior colliculus. II. Stimulus intensity effect. Hear. Res. 13:
175-188, 1984a.
MOORE, D. R., SEMPLE, M. N., ADDISON, P. D., ANDAITKIN, L. M. Properties of spatial receptive fields in the central nucleus of the cat inferior
colliculus. I. Responses to tones of low intensity. Hear. Res. 13: 159174, 1984b.
MUSICANT, A. D., CHAN, J. C. K., AND HIND, J. E. Direction-dependent
spectral properties of cat external ear: new data and cross-species comparisons. J. Acoust. Sot. Am. 87: 757-78 1, 1990.
PARK, T. J. AND POLLAK, G. D. GABA shapes sensitivity to interaural
intensity disparities in the mustache bat’s inferior colliculus: implications for encoding sound location. J. Neurosci. 13: 2050-2067, 1993.
PHILLIPS, D. P. AND IRVINE, D. R. F. Responses of single neurons in physiologically defined area AI of cat cerebral cortex: sensitivity to interaural
intensity differences. Hear. Res. 4: 299-307, 198 1.
PHILLIPS, D. P. AND IRVINE, D. R. F. Some features of binaural inputs to
single neurons in physiologically defined AI of cat cerebral cortex. J.
Neurophysiol. 49: 383-395, 1983.
RAJAN, R., AITKIN, L. M., AND IRVINE, D. R. F. Azimuthal sensitivity of
neurons in primary auditory cortex of cats. I. Types of sensitivity and the
2216
F. IS. SAMSON,
P. BARONE,
effects of variations in stimulus parameters. J. Neurophysiol. 64: 872887, 1990.
REALE, R. A. AND BRUGGE, J. F. Auditory cortical neurons are sensitive to
static and continuously changing interaural phase cues. J. Neurophysiol.
64: 1247-1260, 1990.
REALE, R. A. AND KETTNER, R. E. Topography ofbinaural organization in
primary auditory cortex in the cat: effects of changing interaural intensity. J. Neurophysiol. 56: 663-682, 1986.
ROSE, J. E., GROSS, N. B., GEISLER, C. D., AND HIND, J. E. Some neuronal
mechanisms in the inferior colliculus of the cat which may bc relevant to
localization of a sound source. J. Neurophysiol. 29: 288-3 14, 1966.
SALLY, S. L. AND KELLY, J. B. Effects of superior olivary complex lesions
on binaural responses in rat inferior colliculus. Brain Rex 572: 5-18,
1992.
SAMSON, F. R. AND IMIG, T. J. Physiological mechanisms of directional
selectivity in the cat’s primary auditory cortex (AI) revealed by ear occlusion. Sot. Neurosci. Abstr. 16: 299.19, 1990.
SAMSON, F. K., CLAREY, J. C., BARONE, P., AND IMIG, T. J. Effects of ear
plugging on single-unit azimuth sensitivity in cat primary auditory cortex. I. Evidence for monaural directional cues. J. Neurophysiol. 70: 49251 1, 1993.
SANCHEZ-L• NGO, L. P. AND FORSTER, F. M. Clinical significance of impairment of sound localization. Neurology 8: 119-l 25, 1958.
SEMPLE, M. N., AITKIN, L. M., CALFORD, M. B., PETTIGREW, J. D., AND
PHILLIPS, D. P. Spatial receptive fields in the cat inferior colliculus.
Hear. Res. 10: 203-215, 1983.
SEMPLE, M. N. AND KITZES, L. M. Binaural processing of sound-pressure
level in the inferior colliculus. J. Neurophysiol. 57: 1130- 1147, 1987.
SEMPLE, M. N. AND KITZES, L. M. Binaural processing of sound pressure
J. C. CLAREY,
AND
T. J. IMIG
level in cat primary auditory cortex: evidence for a representation based
on absolute levels rather than interaural level differences. J. Neurophysiol. 69: 449-46 1, 1993a.
SEMPLE, M. N. AND KITZES, L. M. Focal selectivity for binaural soundpressure level in cat primary auditory cortex: two-way intensity network
tuning. J. Neurophysiol. 69: 462-473, 1993b.
SIEGEL, S. Nonparametric
Statistics:
For the Behavioral
Sciences, New
York: McGraw-Hill,
1956.
SOVIJ~RVI, A. R. S. AND HYV;~RINEN, J. Auditory cortical neurons in the
cat sensitive to the direction of sound source movement. Brain Res. 73:
455-471,1974.
STILLMAN, R. D. Responses of high-frequency inferior colliculus neurons
to interaural intensity differences. Exp. Neural. 36: 11% 126, 1972.
TSUCHITANI, C. Functional organization of lateral cell groups of cat superior olivary complex. J. Neurophysiol. 40: 296-3 18, 1977.
WISE, L. Z. AND IRVINE, D. R. F. Auditory response properties of neurons
in deep layers of cat superior colliculus. J. Neurophysiol. 49: 674-684,
1983.
WISE, L. Z. AND IRVINE, D. R. F. Interaural intensity difference sensitivity
based on facilitatory binaural interaction in cat superior colliculus.
Hear. Res. 16: 181-187, 1984.
WISE, L, Z, AND IRVINE, D. R, F. Topographic organization of interaural
intensity difference sensitivity in deep layers of cat superior colliculus:
implications
for auditory spatial representation. J. Neurophysiol.
54:
185-211, 1985.
YIN, T. C. T., CHAN, J. C. K., AND IRVINE, D. R. F. Effects of interaural
time delays of noise stimuli on low-frequency cells in the cat’s inferior
colliclus. I. Responses to wideband stimuli. J. Neurophysiol. 55: 280300, 1986.