Neuron
midbrain responses, suggesting a subcortical originfor robust sound localization in reverberant environ-
ments.
INTRODUCTION
The ability to localize sound sources can be important for survival
and facilitates the identification of target sounds in multisource
environments (Darwin, 2008; Kidd et al., 2005; Shinn-Cunning-
ham, 2008). The auditory scenes that we perceive unfold in envi-
ronments full of surfaces like walls, trees, and rocks (Huisman
and Attenborough, 1991; Sakai et al., 1998). When an acoustic
wave emanating from a sound source strikes a boundary
surface, a fraction of the energy is reflected. The reflected waves
Shinn-Cunningham et al., 2005b), suggesting that listeners are
not immune to the ongoing, corrupted directional cues. To
date, no one has studied the directional sensitivity of auditory
neurons using stimuli with realistic reverberation. Thus, the
degree to which auditory neurons maintain robust directional
sensitivity in reverberation is unknown.
ITDs are initially coded in the auditory pathway as differences
in relative spike timing between auditory nerve fibers on the left
and right sides of the head. These timing differences are trans-
formed to a rate code in the medial superior olive (MSO), where
morphologically and physiologically specialized neurons (Grothe
and Sanes, 1994; Scott et al., 2005; Smith, 1995; Svirskis et al.,
2004) perform coincidence detection on convergent input from
both sides of the head (Goldberg and Brown, 1969; Yin and
Chan, 1990). Theoretically, the average firing rate of these coin-Article
Accurate Sound Localizatio
Environments Is Mediated b
of Spatial Cues in the Audit
Sasha Devore,
1,2,
* Antje Ihlefeld,
3
Kenneth Hancock,
1
Barba
1
Eaton Peabody Laboratory, Massachusetts Eye & Ear Infirmary, Bos
2
Harvard-MIT Division of Health Sciences and Technology, Cambridg
3
Hearing Research Center, Boston University, Boston, MA 02108, US
4
Research Laboratory of Electronics, Massachusetts Institute of Tech
*Correspondence: sashad@alum.mit.edu
DOI 10.1016/j.neuron.2009.02.018
SUMMARY
In reverberant environments, acoustic reflections
interfere with the direct sound arriving at a listener’s
ears, distorting the spatial cues for sound localiza-
tion. Yet, human listeners have little difficulty local-
izing sounds in most settings. Because reverberant
energy builds up over time, the source location is rep-
resented relatively faithfully during the early portion of
a sound, but this representation becomes increas-
ingly degraded later in the stimulus. We show that
the directional sensitivity of single neurons in the
auditory midbrain of anesthetized cats follows
a similar time course, although onset dominance in
temporal response patterns results in more robust
directional sensitivity than expected, suggesting
a simple mechanism for improving directional sensi-
tivity in reverberation. In parallel behavioral experi-
ments, we demonstrate that human lateralization
judgments are consistent with predictions from
a population rate model decoding the observedthemselves generate second-order reflections, with the process
repeating ad infinitum. The myriad of temporally overlapping
reflections, perceived not as discrete echoes but as a single
acoustic entity, is referred to as reverberation.n in Reverberant
y Robust Encoding
ory Midbrain
ra Shinn-Cunningham,
2,3
and Bertrand Delgutte
1,2,4
ton, MA 02114, USA
e, MA 02139, USA
A
nology, Cambridge, MA 02139, USA
Reverberation poses a challenge to accurate sound localiza-
tion. To estimate the location of a sound source with low-
frequency energy, such as speech, human listeners rely princi-
pally on tiny interaural time differences (ITDs) that result from
the separation of the ears on the head (Macpherson and Middle-
brooks, 2002; Wightman and Kistler, 1992). In a reverberant envi-
ronment, reflected acoustic waves reach the listener from all
directions, interfering with the direct sound. Under such condi-
tions, the ear-input signals become decorrelated (Beranek,
2004) and the instantaneous ITD fluctuates (Shinn-Cunningham
and Kawakyu, 2003). Because reverberant energy builds up over
time, the directional information contained in the ear-input
signals has a characteristic time course, in that ITD cues repre-
sent the true source location relatively faithfully during the early
portion of a sound, but become increasingly degraded later in
the stimulus.
In principle, listeners could accurately localize sounds in rever-
beration by basing their judgments on the directional information
in the uncorrupted onset of the signals reaching the ears.
Although human listeners can robustly localize sound sources
in moderate reverberation (Hartmann, 1983; Rakerd and Hart-
mann, 2005), localization accuracy degrades in stronger rever-
beration (Giguere and Abel, 1993; Rakerd and Hartmann, 2005;cidence detectors is equivalent to a crosscorrelation of the input
spike trains (Colburn, 1973).
The majority of neurophysiological studies of spatial process-
ing have targeted the inferior colliculus (IC), the primary nucleus
Neuron 62, 123–134, April 16, 2009 ª2009 Elsevier Inc. 123

et al., 1999; Joris, 2003; Kuwada et al., 1987; Kuwada and Yin, acoustics of a medium-size room (e.g., a classroom) and were
p
w
b
s
c1983; McAlpine et al., 2001; Rose et al., 1966; Stillman, 1971a;
Yin et al., 1986). Multiple parallel sound-processing pathways in
the auditory brainstem converge in the IC (Adams, 1979; Oliver
et al., 1995), making it a site of complex synaptic integration.
Despite this complexity, the rate responses of low-frequency,
ITD-sensitive IC neurons to broadband signals with a static inter-
aural delay resemble the responses of ITD-sensitive neurons in
the MSO (Yin et al., 1986) and are well modeled as a crosscorrela-
tionof the acoustic ear-input signals, after accounting for cochlear
frequency filtering (Hancock and Delgutte, 2004; Yin et al., 1987).
Here, we investigate the effects of reverberation on the direc-
tional sensitivity of low-frequency ITD-sensitive IC neurons.
Consistent with the buildup of reverberation in the acoustic
inputs, we show that directional sensitivity is better near the onset
of a reverberant stimulus and degrades over time, although direc-
tional sensitivity is more robust than predictions from a traditional
crosscorrelation model of binaural processing that is insensitive
to temporal dynamics in the reverberant sound stimuli. We further
show that human lateralization judgments in reverberation are
consistent with predictions from a population rate model for de-
coding the observed midbrain responses, suggesting that robust
encoding of spatial cues in the auditory midbrain can account for
human sound localization in reverberant environments.
RESULTS
Effects of Reverberation on Neural Azimuth Sensitivity
designed to contain only ITD cues, without any interaural level
differences or spectral cues. Stimuli were synthesized for two
distances between the sound source and the virtual ears (1 m
and 3 m) in order to vary the amount of reverberation (‘‘moderate’’
and ‘‘strong’’). The ratio of direct to reverberant energy (D/R)
decreased with increasing distance and was largely independent
of azimuth for each distance simulated (Figure 1C). Reverberation
did not systematically alter the broadband ITD, estimated as the
time delay yielding the maximum normalized interaural correla-
tion coefficient (IACC) between the left and right ear-input signals
(Figure 1D). However, increasing reverberation did cause
a systematic reduction in the peak IACC (Figure 1D, inset), indi-
cating increasing dissimilarity in the ear-input waveforms.
Figures 2A–2C illustrates anechoic (i.e., ‘‘no reverb’’) and
reverberant rate-azimuth curves for three IC units. For anechoic
stimuli (Figures 2A–2C, black curves), the shape of the rate-
azimuth curve was determined by the unit’s sensitivity to ITD
within the naturally occurring range (see Figures S1A and S1B
available online), which corresponds to ± 360 ms for our virtual
space simulations for cats. In many neurons, the discharge
rate increased monotonically with azimuth (Figures 2A and 2B),
particularly in the sound field contralateral to the recording site,
which corresponds to positive azimuths. Units with a nonmono-
tonic dependence of firing rate on azimuth (Figure 2C) generally
peaked within the contralateral hemifield, consistent with the
contralateral bias in the representation of ITD in the mammalian
midbrain (Hancock and Delgutte, 2004; McAlpine et al., 2001;comprising the auditory midbrain (Aitkin et al., 1984; Delgutte
Figure 1. Properties of the Virtual Auditory Space Simulations
(A) Geometry of the virtual auditory environment. Reverberant binaural room im
receiver (1 m and 3 m). Anechoic (i.e., ‘‘no reverb’’) BRIR were created by time-
(B) To simulate a sound source at a given azimuth, a reproducible 400 ms broad
experimental subject over headphones.
(C) Direct to reverberant energy ratio (D/R) versus azimuth for reverberant BRIR
(D) Broadband ITD versus azimuth for each room condition, estimated as the tim
(IACC). Inset, peak IACC for each room condition. Error bars represent ±1 SD aWe used virtual auditory space simulation techniques (Figure 1;
Experimental Procedures) to study the directional response
properties of 36 low-frequency, ITD-sensitive neurons in the IC
124 Neuron 62, 123–134, April 16, 2009 ª2009 Elsevier Inc.of anesthetized cats. The virtual space stimuli simulated the
ulse responses (BRIR) were simulated at two distances between source and
indowing the direct wavefront from the 1 m reverberant BRIR.
and noise burst is convolved with the left and right BRIR and presented to the
.
e delay corresponding to the peak normalized interaural correlation coefficient
ross azimuths.
Neuron
Sound Localization in ReverberationYin et al., 1986).
In reverberation, there was an overall tendency for the range of
firing rates across azimuths to decrease with increasing