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The time course of auditory looming cues in redirecting visuo-spatial attention

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By orienting attention, auditory cues can improve the discrimination of spatially congruent visual targets. Looming sounds that increase in intensity are processed preferentially by the brain. Thus, we investigated whether auditory looming cues can orient visuo-spatial attention more effectively than static and receding sounds. Specifically, different auditory cues could redirect attention away from a continuous central visuo-motor tracking task to peripheral visual targets that appeared occasionally. To investigate the time course of crossmodal cuing, Experiment 1 presented visual targets at different time-points across a 500 ms auditory cue’s presentation. No benefits were found for simultaneous audio-visual cue-target presentation. The largest crossmodal benefit occurred at early cue-target asynchrony onsets (i.e., CTOA = 250 ms), regardless of auditory cue type, which diminished at CTOA = 500 ms for static and receding cues. However, auditory looming cues showed a late crossmodal cuing benefit at CTOA = 500 ms. Experiment 2 showed that this late auditory looming cue benefit was independent of the cue’s intensity when the visual target appeared. Thus, we conclude that the late crossmodal benefit throughout an auditory looming cue’s presentation is due to its increasing intensity profile. The neural basis for this benefit and its ecological implications are discussed.
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SCIenTIfIC RepoRTS | (2019) 9:743 | DOI:10.1038/s41598-018-36033-8
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The time course of auditory
looming cues in redirecting visuo-
spatial attention
Christiane Glatz1,2 & Lewis L. Chuang1,3
By orienting attention, auditory cues can improve the discrimination of spatially congruent visual
targets. Looming sounds that increase in intensity are processed preferentially by the brain. Thus, we
investigated whether auditory looming cues can orient visuo-spatial attention more eectively than
static and receding sounds. Specically, dierent auditory cues could redirect attention away from a
continuous central visuo-motor tracking task to peripheral visual targets that appeared occasionally.
To investigate the time course of crossmodal cuing, Experiment 1 presented visual targets at dierent
time-points across a 500 ms auditory cue’s presentation. No benets were found for simultaneous
audio-visual cue-target presentation. The largest crossmodal benet occurred at early cue-target
asynchrony onsets (i.e., CTOA = 250 ms), regardless of auditory cue type, which diminished at CTOA
= 500 ms for static and receding cues. However, auditory looming cues showed a late crossmodal
cuing benet at CTOA = 500 ms. Experiment 2 showed that this late auditory looming cue benet was
independent of the cue’s intensity when the visual target appeared. Thus, we conclude that the late
crossmodal benet throughout an auditory looming cue’s presentation is due to its increasing intensity
prole. The neural basis for this benet and its ecological implications are discussed.
Whilst driving a car, we have to concentrate on the road ahead while remaining alert to sudden events in our
visual periphery, such as the sudden appearance of a jaywalking pedestrian. Fortunately, we are well-equipped
to deal with the abrupt appearance of such critical events. ey involuntarily and rapidly attract attention to
themselves1 and confer faster and more accurate processing to spatially coincident events that follow thereaer27.
Reexive orienting can occur crossmodally. Like visual events, auditory events can similarly capture visuo-spatial
attention and confer cuing benets to visual targets within spatial proximity810. However, this involuntary ori-
enting of spatial attention is transient and is not sustained indenitely. Especially, if attention is required else-
where—such as, returning to our original example, the road ahead. It is well-established that the time course
of orienting occurs and decays rapidly2,11,12. In fact, observable benets of cuing start to reverse when cues and
targets are separated by durations longer than 300 ms1315. ese known properties of visuo-spatial attention raise
some interesting questions. First, to what extent will an auditory cue reorient and maintain visuo-spatial attention
throughout its own presentation? To date, most studies on crossmodal spatial orienting have employed auditory
cues with short durations (e.g., 83–250 ms)8,9,16. Nonetheless, auditory events (e.g., speech, objects) are typically
characterized by how they change over time. Even simple changes in intensity could signal whether an object is
approaching or departing. us, could spatiotemporal changes in an auditory cue also inuence the time course
by which it redirects visuo-spatial attention? e current work investigates how changes in an auditory cue’s
intensity prole might inuence its ability to redirect visuo-spatial attention. Specically, we report two experi-
ments that demonstrate that auditory looming cues (i.e., sounds with rising intensities) are able to redirect and
sustain visuo-spatial attention until the end of their presentation (Experiment 1), in a way that does not depend
on their intensity levels per se (Experiment 2). In contrast, auditory cues with decreasing or steady-state intensity
proles elicit a rapid deployment of transient attention that does not last throughout their presentation.
Objects appear to approach us when they expand visually or when they get louder with time. Such objects,
termed looming, are claimed to be especially salient because they signal imminent threats. For example, visual
looming objects induce involuntary fear and avoidance responses in mice17, rhesus monkeys18, and human
1Max Planck Institute for Biological Cybernetics, Department Human Perception, Cognition, and Action, Tübingen,
72076, Germany. 2Graduate Training Centre of Neuroscience, University of Tübingen, Tübingen, 72074, Germany.
3Institute for Informatics, Ludwig-Maximilian-Universiät, Munich, 80337, Germany. Correspondence and requests
for materials should be addressed to L.L.C. (email: lewis@humanmachinesystems.org)
Received: 5 April 2018
Accepted: 14 November 2018
Published: xx xx xxxx
OPEN
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infants19, which suggests reexive and innate mechanisms to looming stimuli. e auditory equivalent, namely
looming sounds with rising intensities, have also been associated with preferential processing and alerting
responses. Looming sounds elicit larger skin conductance responses20 and amygdala activity21 than receding
sounds (but see22 for an alternative account in the context of auditory motion in music). Looming sounds with
rising intensities are oen perceived as changing more than their equivalent receding counterparts with falling
intensities21,2326. Moreover, looming sounds are also perceived as having a longer duration than their receding
equivalent2731, which indicate that they might be attended to for longer durations. Finally, looming sounds are
associated with greater activity in the auditory cortex, as well as in neural networks related to attention and spa-
tial processing3234. Taken together, it is generally agreed that looming sounds are salient auditory stimuli that
increase phasic alertness, presumably because they communicate approaching threats24.
e saliency of looming sounds can inuence visual perception. For example, static visual targets are perceived
as larger or brighter than they really are, when accompanied by looming sounds35. In a more realistic setting,
drivers braked earlier if a potential head-on collision was accompanied with a looming sound, relative to a static
auditory warning36. More interestingly, auditory looming stimuli can induce excitation in visual cortical regions
for low-level processing37,38. ese interactions are oen discussed in terms of multisensory integration38,39.
Nonetheless, there is some evidence that looming sounds can also exert a preferential bias on visuo-spatial atten-
tion. When presented in only one ear, a looming sound can increase tilt discrimination sensitivity in the congru-
ent visual hemield relative to the opposing hemield, for an object that is presented simultaneously16. is raises
the question: What is the role (if any) of a looming sound in reorienting visuo-spatial attention?
Looming sounds are salient events that can enhance the perception of visual targets37, especially targets that
are spatially congruent16. In the current study, we investigate whether auditory looming cues might exert a cross-
modal inuence on visuo-spatial attention, across its presentation duration, in a way that might dier from other
similar auditory cues. In particular, we contrast looming sounds against sounds with a steady-state intensity or a
decreasing intensity prole. If looming sounds are salient and exert a strong bottom-up inuence on reorienting
visuo-spatial attention, we expect cuing benets to be larger at short cue-target onset asynchronies (CTOAs; i.e.,
250 ms) compared to other auditory cues. Independent of cuing benets, auditory looming sounds might even
improve the discrimination of simultaneously presented visual targets (cf., Leo et al.16), given that they are known
to generally facilitate visual processing37,38. In both cases, such cuing benets of reexive visuo-spatial attention
can be expected to diminish with time and, potentially, throughout the presentation of the sounds themselves. On
the other hand, the ongoing presentation of looming sounds (but not static and receding sounds) might indicate
the continuous approach of a visual target, motivating participants to not only redirect but to sustain their atten-
tion40. is would result in cuing benets that last until the end of the auditory cue’s presentation.
Experiment 1 varied the CTOAs between different auditory cues and the visual target of a peripheral
tilt-discrimination task. However, it has to be noted that looming cues were physically louder than the static and
receding cues at the end of their presentation. Furthermore, previous studies have shown that looming sounds
also tend to be perceived as louder4143 and longer-lasting2731 than their receding equivalents, perhaps due to a
recency eect25,26. Given that the looming cue benet at 500 ms CTOA could have resulted from the intensity
dierences between the auditory cues at 500 ms, Experiment 2 manipulated the nal intensity levels of static
and looming cues and compared their cuing benets at a xed CTOA of 500 ms. Experiment 2 veried that the
cuing benet of auditory looming cues, unlike auditory static cues, was independent of their respective intensities
when the visual target appeared. Two key aspects set the current study apart from previous research. Unlike most
studies on spatial orienting, we employed a dual-task paradigm that required participants to perform a central
manual tracking task at all times. In other words, diverting spatial attention away from the central location comes
at a cost, which can reasonably be assumed to be larger than if participants were merely requested to maintain
central xation. Another distinction is the use of looming sounds as a spatially valid cue to direct attention to the
location of an upcoming target.
e current experiments were designed to examine how sounds govern visuo-spatial orienting through-
out their presentation. Hence, we employed auditory cues with durations that were longer than comparable
audio-visual crossmodal cuing studies8,9 and presented visual targets at dierent points across their presentation
duration. In this regard, our experiment design diers from previous work that have similarly addressed the
crossmodal inuence of looming sounds on visual processing. To begin, previous studies have typically presented
a visual target simultaneously with the onset of a looming sound16,38,39,44,45 or aer a looming sound has been pre-
sented20,21. e former paradigm typically addressed supramodal inuences of looming sounds on multisensory
integration and the latter, aspects related to phasic alerting. Few studies16 have directly investigated how looming
sounds inuence visuo-spatial attention. erefore, the current study is the rst to describe the time course of an
auditory cue’s crossmodal inuence on orienting visuo-spatial attention.
Experiment 1: Do auditory looming sounds enhance peripheral tilt-discrimination
performance across its presented duration?
Results and Discussion. Performance in the peripheral tilt-discrimination task was operationalized
in terms of the time that a participant took to respond correctly from the time of target appearance (RTs).
Participants responded on average 72.7% of the times correct. To compensate for positive skews in RT measures46,
medians RTs were calculated for each experimental condition. is data is presented in Fig.1. ere is a gen-
eral pattern of cuing benets, irrespective of auditory cue types, that peaks for visual targets that appear 250 ms
aer the onset of the auditory cue and diminish for those that appear 500 ms aer cue onset. Interestingly, there
appears to be no benet for the discrimination of visual targets that appear simultaneously with the auditory cues.
e median RTs were submitted to a repeated measures ANOVA (JASP47; see Supplementary Material) for
the factors of Auditory Cue (none, looming, receding, static) and CTOA (0, 250, 500 ms). ere was signicant
interaction between the factors of Auditory Cue and CTOA (F(6, 84) = 13.383, p = 0.001, ω2 = 0.449) as well as
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for both main eects (Auditory Cue: (F(3, 42) = 20.553, p = 0.001, ω2 = 0.560); CTOA: (F(1.374, 19.242) = 9.155,
p = 0.004, ω2 = 0.345). To interpret the interaction, we performed separate one-way ANOVAs for the factor of
CTOA for each auditory cue condition. With the exception of the ‘none’ condition, all conditions returned a sig-
nicant main eect for CTOA. For auditory static cues, signicantly faster RTs were found at a CTOA of 250 ms,
compared to 0 ms (t(14) = 4.746, pbonf <0.001, d = 1.226) and 500 ms (t(14) = 2.798, pbonf = 0.028, d = 0.722).
Auditory receding cues showed a similar pattern of faster RTs at a CTOA of 250 ms, compared to 0 ms (t(14) =
5.152, pbonf <0.001, d = 1.330) and 500 ms (t(14) = 4.354, pbonf <0.001, d = 1.124). e RTs between CTOAs of
0 ms and 500 ms neither diered for auditory static cues (t(14) = 1.949, pbonf = 0.184, d = 0.503) nor auditory
receding cues (t(14) = 0.798, pbonf = 1.000, d = 0.206). In contrast, auditory looming cues showed a dierent
pattern of RTs across CTOA levels. Compared to a CTOA of 0 ms, RTs were signicantly faster at both CTOAs of
250 ms (t(14) = 4.471, pbonf <0.001, d = 1.154) and 500 ms (t(14) = 2.971, pbonf =0.018, d = 0.767). Interestingly,
RTs did not dier signicantly between CTOAs of 250 ms and 500 ms (t(14) = 1.500, pbonf =0.434, d = 0.387).
Finally, we contrasted the median RTs of the three cue conditions at the CTOA level of 500 ms with two-tailed
paired-samples t-tests. Looming cues gave rise to faster RTs at 500 ms than receding cues (t(14) = 2.281, p =
0.039, d = 0.589). ere were no signicant dierences between static and looming cues (t(14) = 0.965, p = 0.351,
d = 0.249), and static and receding cues (t(14) = 1.199, p = 0.250, d = 0.310).
Discrimination sensitivity48 (d) were submitted to the same repeated measures ANOVA to determine if there
were speed-accuracy tradeos across the cued conditions. ere were no signicant main eects for Auditory Cue
(F(3, 42) = 0.304, p = 0.823, ω2 = 0.000) and CTOA (F(2, 28) = 0.023, p = 0.372, ω2 = 0.002). ere was also no
signicant interaction for Auditory Cue and CTOA (F(6, 84) = 0.739, p = 0.620, ω2 = 0.000).
e root-mean-squared-error (RMSE) of manual tracking during auditory cue presentation was also eval-
uated to determine if the cues impaired central task performance. ere were no signicant main eects of
Auditory Cue (F(3, 42) = 0.938, p = 0.431, ω2 = 0.000), CTOA (F(2, 28) = 0.533, p = 0.539, ω2 = 0.000), or their
interaction (F(6, 84) = 1.393, p = 0.227, ω2 = 0.025).
e results of Experiment 1 reveal that auditory cues can induce a crossmodal reorienting of spatial attention
that result in faster tilt-discriminations of peripheral targets. In a dual-task paradigm with a central task that
demands attention continuously, this manifests itself as a response time benet, with no inuence on discrimina-
tion sensitivity and at no noticeable cost to central task performance. Generally, this crossmodal benet is tran-
sient. It peaks when the visual targets appear shortly aer auditory cue onset at a CTOA of 250 ms and diminishes
with extended cue presentation at a CTOA of 500 ms. Contrary to our expectations, auditory looming cues did
not exhibit cuing benets that were generally stronger compared to the static or receding cue. At 250 ms CTOA,
all auditory cues resulted in comparable cuing benets relative to the simultaneous presentation of auditory cue
and visual target at CTOA 0 ms. Interestingly, there continued to be a cuing benet for auditory looming cues
at a CTOA of 500 ms that signicantly diered from CTOA 0 ms, but not from CTOA 250 ms. is pattern of
results was not observed for the static and receding cued trials that demonstrated a cuing benet only at CTOA
250 ms. Hence, we propose that looming cues result in a cuing benet that does not diminish as readily as static
and receding cues. Nonetheless, these results could also be explained by the intensity of auditory cues at visual
target onset. A comparison of the RTs at 500 ms CTOA reveal a signicant dierence between the loudest (i.e.,
looming) and soest (i.e., receding) cues, but not between these extremes and the cue with intermediate intensity
(i.e., static). Regardless of either explanation, the current results eliminate the possibility that changes in audi-
tory intensity over time (i.e., auditory motion) can, in themselves, result in preferential cuing benets. e next
Figure 1. Interaction of Auditory Cue and CTOA. Cued reaction times are fastest for the CTOA level of 250 ms,
relative to the simultaneous presentation (0 ms) of cue and target. is reaction time benet decreases at 500 ms,
particularly for static and receding cues. Error bars represent 95% condence intervals according to70.
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experiment seeks to clarify if cue benets at long CTOA (i.e., 500 ms) ought to be attributed to cue intensity or
their looming characteristic.
Experiment 2: Can the sustained performance benet of a looming sound at late
CTOAs be attributed to its high intensity when the visual target appears?
Experiment 1 demonstrated that looming sounds exert a signicant crossmodal cue benet to visual targets that
subsequently appeared at either CTOAs 250 ms and 500 ms, compared to when they appeared simultaneously
with the visual target (i.e., CTOA 0 ms). In contrast, the crossmodal cue benet for receding and static sounds was
only signicant at CTOA 250 ms but not at 500 ms, compared to simultaneous presentation with the visual target.
Taken together, this suggests that looming sounds exert a similar reorienting eect as other sounds (i.e., 250 ms),
but unlike other sounds maintains this attention for longer. Nonetheless, a direct comparison of the cue benets at
CTOA 500 ms suggested that the nal intensity (i.e., loudness) of the sounds could have played a supplementary
role in maintaining attention at long CTOAs. Specically, the late crossmodal cue benet (i.e., CTOA 500 ms)
of looming sounds was signicantly larger than the receding sound, though not in comparison to static sound
whose cue benet did not dier from either the receding or looming sounds.
Experiment 2 was designed to discriminate between the inuence of sound intensity and cue type on late
crossmodal cue benets (i.e., CTOA 500 ms). erefore, we varied for the independent variables of Intensity (so,
loud) and Auditory Cue (static, looming). e so-static and loud-looming cues were identical to the static and
looming sounds of Experiment 1. eir cue benets are represented in Fig.2 with larger icons. ere were two
new auditory cues. e steady-state intensity of the loud-static cue was equivalent to the oset intensity of the
original looming sound. e oset intensity of the so-looming cue was equivalent to the steady-state intensity of
the original static sound. To reiterate, Experiment 2 was designed to determine if the late crossmodal cue benets
exhibited by looming sounds were due to their nal intensity levels.
Results and Discussion. To begin, we performed one-tailed paired samples t-tests (α = 0.05) and con-
rmed that all auditory cues induced a late crossmodal cue benet on visual targets (range of means = 664–
688 ms), compared to instances when targets were not preceded by an auditory cue (mean = 736 ms; SE = 79).
Figure2 summarizes the RTs across the conditions that presented an auditory cue. Auditory looming cues appear
to induce a cuing benet that does not change with intensity levels, while a loud-static cue induces a larger cuing
benet than a so-static cue.
e median RTs of Experiment 2 (Fig.2) were submitted to a repeated-measures ANOVA for the factors of
Auditory Cue (static, looming) and Intensity (so, loud). ere were no signicant main eects of Auditory Cue
(F(1, 14) = 0.230, p = 0.639, ω2 = 0.000) and Intensity (F(1, 14) = 1.486, p = 0.243, ω2 = 0.029). More impor-
tantly, this analysis revealed a signicant interaction (F(1, 14) = 7.305, p = 0.017, ω2 = 0.000), conrming our
interpretation of the cuing benets of the dierent auditory cues.
The soft-static cues and loud-looming cues were respectively equivalent to the static and looming cues
employed in Experiment 1. Planned two-tailed paired-samples t-tests revealed a signicant dierence between
the cuing benets of so-static and so-looming (t(14) = 2.220, p = 0.043, d = 0.573), and no signicant dif-
ference between loud-looming and loud-static cues (t(14) = 1.156, p = 0.267, d = 0.298). In other words, the
Figure 2. Interaction of Auditory Cue and Intensity. Median RTs of looming cues do not vary with Intensity
levels. In contrast, loud static cues induce faster RTs than so static cues. e conditions indicated by larger
icons were identical to the static and looming conditions in Experiment 1. Error bars represent 95% condence
intervals according to70.
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looming sounds confer a late crossmodal cue benet regardless of their intensity levels. In contrast, the late cross-
modal cue benet of static cues appear to be depend on their intensity levels.
e same analyses were performed on d scores. Paired samples t-tests conrmed that none of the auditory
cues improved discrimination sensitivity (range of means = 1.680–1.781) relative to uncued trials (mean = 1.653,
SE = 0.206). e ANOVA revealed no signicant main eects and interactions for the factors of Auditory Cue and
Intensity.
Similarly, we analyzed the RMSE on the visuo-motor tracking task to check for interference from auditory
cues. Paired samples t-tests conrmed that none of the auditory cues signicantly reduced central task perfor-
mance (range of means = 1.374–1.438), relative to comparable periods when no cue was presented (mean = 1.407,
SE = 0.082). e ANOVA revealed no signicant main eects and interactions for the factors of Auditory Cue and
Intensity.
To summarize, we found that auditory looming cues confer similar magnitudes of late crossmodal cue benets
at the end of their presentation. In other words, Experiment 1s results cannot be solely attributed to the looming
cue’s loudness levels when the visual target appeared.
Discussion
e current results reveal that looming sounds attract visuo-spatial attention to their locations and confer, regard-
less of their loudness, an early and late crossmodal cue benet. In contrast, comparable sounds (i.e., static and
receding sounds) introduce an early cue benet that wanes, even during their presentation. Although auditory
cue intensity could inuence the magnitude of cue benets over time, this did not appear to be the reason for
looming sound’s persistent cue benet. In fact, a looming sound that ends loudly elicits a cue benet that is
indistinguishable from a looming sound that ends soly. In contrast, the cue benet of static sounds is highly
dependent on the cues steady-state intensities. Hence, we believe that looming sounds exert a unique crossmodal
inuence on visuo-spatial attention; they draw visuo-spatial attention to themselves as well as compel it to remain
for the entirety of their presentation. is holds, even when visuo-spatial attention is demanded elsewhere—that
is, in our study, a central manual tracking task.
At rst glance, our results dier from those reported by Leo and colleagues16. To recap, Leo et al.16 reported
that monoaural auditory looming cues induce a preferential bias in tilt-discrimination sensitivity of the visual
hemield that is spatially congruent to the presentation ear, relative to the hemield that is incongruent. However,
we only found RT benets when the auditory cues preceded visual targets and not when they appeared simul-
taneously with the visual targets (i.e., 0 ms CTOA). Several dierences exist between our experiments. Unlike
Leo and colleagues, we sought to investigate how a crossmodal inuence of auditory cues on spatially congruent
visual targets might operate throughout their presentation. erefore, we varied the CTOAs of auditory cues and
peripheral visual targets, without varying spatial congruency. In contrast, Leo et al.16 evaluated the crossmodal
inuence of non-predictive sounds on simultaneously presented visual targets, which were either spatially con-
gruent or incongruent. It should be noted that Leo et al.16 reported a signicant interaction of sound type and
spatial congruency, but not a main eect of either factors. In other words, Leo et al.s results were similar to our
ndings at 0 ms CTOA, namely that a looming sound or a spatially congruent sound does not, in itself, facilitate
responses to a simultaneously presented visual target in the periphery—that is, not unless it is contrasted to per-
formance in the opponent hemield.
Why do looming sounds continue to confer a crossmodal cue benet that persists until the end of their pres-
entation, when static and receding sounds do not? e attentional mechanisms that underlie spatial orienting can
be dichotomized into those that are early, involuntary, and transient, as opposed to those that are late, voluntary,
and sustained49. From this perspective, looming sounds do not dier from other sounds insofar as they similarly
support the early orienting of attention. However, our results suggest that looming sounds dier in terms of how
they might counteract the withdrawal of early visuo-spatial attention, regardless of their loudness, perhaps by
invoking late and voluntary processes. e current results demonstrate that looming sounds are dierent from
receding and static sounds by conferring a late crossmodal cue benet that is apparent at the end of their duration.
Critically, this does not depend on their actual intensity, but rather how their intensity increases with time. e
rest of this discussion will address the various explanations for why this is so.
e intuitive argument that looming sounds are ecologically salient and, hence, raise overall arousal cannot
fully account for our current ndings. If this was true, we would have expected response times to be faster when-
ever looming sounds accompanied visual targets. is might even have given rise to more false positives and,
hence, lower sensitivity scores. Instead, our results demonstrate that looming sounds selectively dierentiate
from receding and static sounds with regards to how they confer a persistent cue benet. Previous studies in
multisensory integration have demonstrated that looming sounds can generally improve visual stimulus process-
ing16,38,39,44,45. Nonetheless, our participants were not better at discriminating visual targets that appeared with
the onset of looming sounds compared to when looming sounds preceded visual targets (see Fig.1). erefore,
we are condent that our current ndings relate to crossmodal inuence of sounds on reorienting visuo-spatial
attention, and not to multisensory integration. An argument for ecological saliency might also suggest stronger
reexive orienting. If this was true, looming sounds ought to have induced larger early cue benets at the CTOAs
of 250 ms. However, this does not appear to be true (see Fig.1). In contrast, increasing the salience (i.e., inten-
sity) of static sounds increased the magnitude of their late crossmodal cue benet, but not for looming sounds
(Experiment 2). erefore, an ecological saliency account does not apply to our current ndings even though we
do not dispute that looming stimuli might still be preferentially processed because they: induce larger skin con-
ductance responses20, elicit faster detection39,50,51, preferentially activate limbic21 as well as cortical33 structures,
and are subjectively rated as being highly arousing20.
Looming sounds can be perceived as being louder than comparable static and receding sounds25,26. is is
due to a recency eect, whereby observers respond to the sounds nal instead of their overall intensity over time.
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However, Experiment 2 allows us to rule out this explanation, given that it manipulated cue intensity directly and
found no dierence in the late crossmodal cue benets of so and loud looming sounds. erefore, we do not
believe that the late crossmodal cue benet of looming sounds is due to their perceived loudness.
Looming sounds can also be perceived as lasting longer than their receding equivalents2731. To begin, the
end of a receding sound may be suppressed because it is perceived as irrelevant reverberations of the sound
ratherthan being part of the sound itself52. Alternatively, listeners might ignore the end of a receding sound given
that they are expected to fade eventually29, unlike looming sounds that could rise indenitely depending on their
source intensity. Certainly, receding cues that are perceived as ending earlier can be expected to motivate earlier
shis of reoriented attention back to the manual tracking task. Nonetheless, it is unclear if this explanation can
be directly applied to the duration perceptions of static and looming sounds. In fact, previous work have reported
the perceived duration of looming sounds to be equivalent to static sounds31 or even shorter29. To the best of our
knowledge, the perceived durations oflooming sounds have yet to be reported as being longer than static sounds.
Finally, we could explain our current ndings in terms of the anticipation that looming sounds might elicit
in our observers for an approaching object, as long as the looming sound persists. In contrast, receding sounds
signal a departing object and static sounds, a stationary object. Looming sounds provide information about object
motion. More specically, they indicate the intrusion of objects into the immediate space surrounding ones body
(i.e., peripersonal space; PPS). Previous work has shown that approaching sounds receive even more attention
when entering one’s PPS than when approaching at further distance53. is could also explain why auditory loom-
ing cues in our study might support late mechanisms of attention orienting, while not diering from other cues
with regards to early mechanisms. Looming sounds that continue to increase in intensity are more likely to indi-
cate greater personal relevance. Furthermore, previous work has also found that looming objects can extend our
perceived PPS boundaries54,55 and, in doingso, preserve a larger margin of safety around the body. is selective
concern for looming objects could explain why looming sounds receive attention as long as they continue to
indicate approach.
As long as a sound increases in intensity, it is suggestive of the time when an approaching object will appear56,57.
Although intensity oentimes determines stimulus saliency, its inuence on attention is likely to be transient if
it remains unchanged. Electrophysiological research in non-human primates have shown that looming sounds
not only aect the primary auditory cortex, but also those areas that are involved in space recognition, auditory
motion perception, as well as attention33,58. Similarly, fMRI studies have also implicated a network of regions
that are selective to looming sounds that are involved in the evaluation of complex object motion (i.e., superior
and middle temporal sulcus)21,32. More recently, an MEG study has shown sustained neural activity in the right
temporo-occipito-parietal junction and bilateral inferior temporal gyrus, which tracked the increasing intensity
of looming sounds with relatively long durations (i.e., 1600 ms). is resulted in signicant dierences against the
neural activity generated by falling intensities of receding sounds, particularly at late periods (i.e., 900–1400 ms)
aer sound onsets. More interesting, these regions are not considered to be part of the auditory cortex, hence
suggesting a supramodal inuence of looming sounds on attention34. Sustained activity in these regions suggest
that looming sounds exert a continuous inuence on attention, as long as they continue to increase in intensity
and indicate the potential approach of a relevant object.
e explanation that approaching objects sustain reoriented attention does not contradict an account of eco-
logical saliency. Instead, it suggests thatlooming sounds can target later voluntary mechanisms of attention,
besides early reexive mechanisms. Indeed, our results indicate that looming sounds mitigate the withdrawal
of early cuing benets rather than enhance them. erefore, our ndings indicate that looming sounds oblige
the visual system to continue paying attention to a region of the visual periphery that would otherwise remain
neglected, especially when attentional resources are demanded elsewhere. In this regard, we believe that our
results depended on the fact that we employed a manual tracking task that constantly demanded visuo-spatial
attention59, thus exacting a signicant cost whenever attention was directed elsewhere.
Our current ndings inform the debate on whether motion stimuli are preferentially attended to because of
their early motion onset6062 or their motion properties (i.e., directionality63,64). e current results can be inter-
preted in favor of the latter. If stimulus change (or motion onset) was the primary driver of attentional shis, we
might even expect receding sounds to exert a larger early cuing benet, given that they decreased in intensity
exponentially. Instead, we nd that the cuing benets of looming sounds discriminate themselves towards the end
of their presentation, namely when they are perceived as being closest to the observer and, hence, most relevant.
In conclusion, the current study reports that looming sounds exert a late crossmodal benet on visuo-spatial
attention that is apparent throughout their presentation. is is in spite of the demands for visuo-spatial attention
by a central manual tracking task. Hence, this study extends the role of auditory looming from multisensory inte-
gration and highlights the role of auditory looming in capturing and reorienting attention away from a primary
task. e important peculiarity of auditory looming in this context is the rising intensity which, independent of
its overall intensity, compels observers to persist in attending to the cued location. Aer all, the gentle prowl of a
tiger can be as deadly as the clumsy stampede of cattle, but only when they near us.
Methods
Participants. irty healthy volunteers participated in the current study (Experiment 1: 7 males, 8 females;
mean age = 26.67 years ±4.78 s.d.; Experiment 2: 5 males, 10 females; mean age = 24.67 years ±3.79 s.d.). All
participants reported normal hearing, normal (or corrected-to-normal) vision, and no history of neurological
problems. ey received written instructions, gave informed signed consent, and were remunerated 8 Euros/
hour for their voluntary participation. e experimental procedure was approved by the Ethics Council at the
University Hospital Tuebingen and carried out in accordance with their specied guidelines and regulations (see
DOI 10.17605/OSF.IO/4WYGJ).
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SCIenTIfIC RepoRTS | (2019) 9:743 | DOI:10.1038/s41598-018-36033-8
Design. Experiments 1 and 2 employed a full factorial repeated measures design. Experiment 1 had two inde-
pendent variables: (1) CTOA between an auditory cue and the peripheral visual target with three levels (either 0,
250, or 500 ms), (2) the intensity prole of the Auditory Cue with four levels (none, static, looming, and receding).
Experiment 2 had two independent variables with two levels each: (1) intensity prole of the Auditory Cue (static,
looming), (2) Intensity of the auditory cue (low, high). e CTOA in Experiment 2 was xed at 500 ms. e pri-
mary dependent variable was the median response time for correct responses to the peripheral target.
Every session consisted of several 4.5 mins blocks of continuous manual tracking with 60 trials of a
single-stimulus forced-choice (1AFC) peripheral tilt-discrimination task. Experiment 1 consisted of three ses-
sions (15 blocks each) performed over consecutive days. CTOA was xed for each block and the presentation
order of CTOA was counterbalanced within sessions and across participants. Experiment 2 was conducted in one
session (i.e., 20 blocks) on a single day.
Stimuli. For Experiment 1, the auditory cues were 400 Hz tones with triangular44 complex waveforms, created
using the MATLAB sawtooth function sampled at 44.1 kHz. eir duration was 500 ms and their intensity over
time was shaped to assume one of three proles: looming, receding, or static. e looming sound was charac-
terized by a dynamic increase from 44 to 68 dB SPL, as measured at the participant’ ear position using an SPL
meter [Brüel & Kjaer, Type 2238]. is change in loudness could be described as an audio object that approaches
at the speed of 29 m/s towards the observer, with a time-to-contact of 500 ms36. e receding sound was created
by reversing the looming sound in time. e static sound had a steady-state intensity that was the mean intensity
level of the looming (and receding) sound, i.e. 56 dB. To avoid clicking noise at sound on- and osets, all sounds
were convolved with a trapezoid grating such that they had 5 ms ramps at the sound on- and oset.
For Experiment 2, the static and looming sounds were modied to create versions that ended with compa-
rable low and high intensities. In Experiment 2, the original looming sound was regarded as the loud-looming
cue and the original static sound as the so-static cue. Accordingly, loud-static cue was the static sound with an
adjusted intensity that matched the loud-looming cues end-intensity of 68 dB, while a so-looming cue was a
looming sound that began ended with an intensity of the original static sound 56 dB and began with an intensity
of 32 dB. ese intensity proles are visualized in Fig.3B. All auditory stimuli can be accessed at DOI 10.17605/
OSF.IO/4WYGJ.
In both experiments, the peripheral visual targets were Gabor patches of 2 degrees visual angle in diameter,
with a spatial frequency of 3.1 cycles/degree and a contrast of 50% (background gray = 20.3 cd/m2, Gabor patch
black = 1.3 cd/m2, Gabor patch white 38.3 cd/m2). ey were always presented 9° to the le or right of the manu-
ally tracked crosshair for 250 ms. A pre-testing adaptive procedure tuned the orientation tilts to be 70% orienta-
tion discrimination threshold of each participant (mean threshold and standard error for the le hemield: 1.74°
± 0.27, and the right hemield: 1.70° ± 0.21)65.
A compensatory visuo-motor tracking task, presented in the center, had to be performed continuously. A
crosshair cursor comprising a vertical and horizontal line (0.70° long) was continuously and vertically displaced
from a dotted horizontal reference line (5.43° long), along the vertical screen center. Participants rejected this
cursor displacement to stabilize this cursor by deecting a joystick forwards and backwards, which controlled
the cursor’s vertical velocity and acceleration with equal weighting. In the absence of manual inputs, the cursor
displacement was controlled by a quasi-random reference signal that was a sinusoidal function comprised of a
sum of ten, non-harmonically related sine waves. is function had a variance of 1.62°66.
Apparatus. e experiment was controlled with custom-written soware in MATLAB 8.2.0.701 (R2013b)
and Psychophysics Toolbox 3.0.126769). A ViewPixx Screen (60.5 × 36.3 resolution; 120 Hz) presented all visual
Figure 3. Experiment procedure and stimuli. (A) Four instances of trials of equal probability that could
require participants to perform tilt-discrimination on a peripheral visual target (depicted larger than actual, for
visibility). (B) Auditory cues used in Experiment 2, whereby the so-static cue and loud-looming cue were the
static and looming cue of Experiment 1. (C) Visual targets could appear at the onset of the auditory cue or aer
the onset.
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8
SCIenTIfIC RepoRTS | (2019) 9:743 | DOI:10.1038/s41598-018-36033-8
stimuli, at a xed distance of 45 cm from chin-rest. Sound presentation was controlled by an ASIO compatible
sound card (SoundBlaster ZxR; Creative Labs) and presented monophonically through either the le or right
speaker of a pair of headphones (MDR-CD380; Sony). e right and le arrow inputs of a standardized keyboard
were used for collecting le and right tilt discrimination responses respectively. A right-handed control stick
(Hotas Warthog Flight Stick) was used for the central manual tracking task.
Procedure. Prior to testing and aer experiment brieng, participants performed ve practice blocks of man-
ual tracking only, followed by an adaptive procedure on a 1AFC tilt-discrimination task on peripheral visual
targets65. e adaptive procedure determined the tilt that corresponded to the participant’s 70% orientation dis-
crimination threshold. Participants xated a static central cross throughout this adaptive procedure. To determine
individual thresholds, we employed a 1-up-2-down staircase procedure with six interleaved staircases, evenly
divided for the le and right hemields. e vertical tilt of the Gabor stimuli had starting values of 0.0°, 2.5°, and
5.0° for three staircases per hemield. Each staircase allowed for a maximum of 100 trials or terminated aer
19 reversals, whichever came rst. e rst four reversals had the respective step sizes of 1.0°, 0.5°, 0.25°, and
0.1°, which then remained constant for the rest of the adaptive procedure. is was always performed in the rst
experimental session.
Upon completion, participants were allowed to perform the test blocks (Experiment 1: n = 45; E xperiment
2: n = 20). Participants were required to perform two concurrent tasks on every test block: (1) a compensatory
manual tracking task on a central crosshair, (2) a 1AFC tilt-discrimination task on peripheral visual targets.
Mandatory 1.5 min rest breaks were provided between blocks.
In the compensatory tracking task, participants deected the right-handed joystick in either the forwards
or backwards direction to their body in order to counteract movements of the crosshair in either the upward or
downward direction respectively. e goal was to stabilize a central crosshair on a horizontal dotted line. In the
tilt-discrimination task, participants had to determine the tilt of peripheral targets when they appeared on either
the le or right side of the crosshair. ey responded by using their le index or ring nger to respectively indicate
a le or right diagonal tilt. Participants were instructed to maintain xation of the central crosshair of the manual
tracking task throughout the experiment.
Trials occurred every 2000 ms ± 1000 ms (uniform distribution) and presented either an auditory cue only
(A-X), a peripheral visual target only (X-V), an auditory cue followed by a peripheral visual target (A-V), or nei-
ther cue nor target (X-X). is ensured that the auditory cue was non-predictive of target appearance. When an
auditory cue was presented, they were always presented via the headphone (i.e., right/le) that was on the same
side as the upcoming visual target. When visual targets were presented, they appeared equally oen on the le and
the right of the central visuo-motor tracking task. In Experiment 1, they could occur at the onset of an auditory
cue (if any), or 250 ms or 500 ms aer the cue onset (see Fig.3C). In Experiment 2, visual targets always appeared
500 ms aer the auditory onset. A xed duration of 2000 ms for keypress responses always took place aer a visual
target was supposed to be presented. e timelines of these four possible trials are illustrated in Fig.3A.
After completing the required number of test blocks, participants were debriefed on the purpose of the
experiment.
Data Availability
e datasets generated during and/or analyzed during the current study are available in the OSF repository,
https://doi.org/10.17605/OSF.IO/4WYGJ.
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Acknowledgements
is work was supported by the German Research Foundation (DFG) within project C03 of SFB/Transregio 161.
We would like to thank Dr. Tonja Machulla, Prof. Dr. Heinrich Bültho, and our two anonymous reviewers for
their helpful comments.
Author Contributions
C.G. and L.L.C. conceived the experiment, C.G. conducted the experiments, C.G. and L.L.C. analyzed the results.
All authors reviewed the manuscript.
Additional Information
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... The results of our study demonstrated that the looming sounds with an adequate duration (i.e., 120 ms) induced PPI enhancement compared with receding sounds with the same duration, suggesting that approaching sounds serve an intrinsic warning cue for individuals to dampen the startle response elicited by a sudden and interfering stimuli. The "auditory looming bias" shown in previous literature (Neuhoff, 2001;Ghazanfar et al., 2002;Seifritz et al., 2002;Hall and Moore, 2003;Maier et al., 2004;Maier and Ghazanfar, 2007;Grassi, 2010;Baumgartner et al., 2017;Glatz and Chuang, 2019;Bidelman and Myers, 2020) was also found in PPI of the acoustic startle response paradigm in rats. We further showed that this looming effect-induced PPI enhancement was time or rate dependent. ...
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... Specifically, auditory cues that increased in intensity facilitated detection of a peripheral visual stimulus presented 500 ms after the auditory cue, compared to cues that decreased in intensity and static auditory cues (Glatz & Chuang, 2019). The authors suggest that the looming auditory cue facilitated sustained attention (Glatz & Chuang, 2019). Taken together, the above experiments demonstrate how temporal preparation can improve perceptual processing. ...
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