Institut für Biologie II, Rheinisch-Westfälische Technische Hochschule Aachen, D-52074 Aachen, Germany
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ABSTRACT |
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Johnen, Anja, Hermann Wagner, and Bernhard H. Gaese. Spatial Attention Modulates Sound Localization in Barn Owls. J. Neurophysiol. 85: 1009-1012, 2001. Attentional influence on sound-localization behavior of barn owls was investigated in a cross-modal spatial cuing paradigm. After being cued to the most probable target side with a visual cuing stimulus, owls localized upcoming auditory target stimuli with a head turn toward the position of the sound source. In 80% of the trials, cuing stimuli pointed toward the side of the upcoming target stimulus (valid configuration), and in 20% they pointed toward the opposite side (invalid configuration). We found that owls initiated the head turns by a mean of 37.4 ms earlier in valid trials, i.e., mean response latencies of head turns were reduced by 16% after a valid cuing stimulus. Thus auditory stimuli appearing at the cued side were processed faster than stimuli appearing at the uncued side, indicating the influence of a spatial-selective attention mechanism. Turning angles were not different when owls turned their head toward a cued or an uncued location. Other types of attention influencing sound localization, e.g., a reduction of response latency as a function of the duration of cue-target delay, could not be observed. This study is the first attempt to investigate attentional influences on sound localization in an animal model.
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INTRODUCTION |
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Several studies have shown that
spatial selective attention can modulate sound localization behavior in
humans (e.g., Mondor and Zatorre 1995; Spence and
Driver 1994
). Using a paradigm adapted from Posner
(Posner et al. 1980
), auditory attention was guided toward desired locations by presenting cuing stimuli prior to the
target stimulus in these studies. It was observed that responses to
auditory events at cued locations are faster compared with responses to
auditory events at uncued locations. The faster processing of auditory
stimuli was related to the different attentional states at cued and
uncued locations.
Investigations of evolutionary constraints on auditory spatial
attention, however, have so far been neglected. We therefore studied
auditory spatial attention at the behavioral level in a
well-established animal model for sound localization, the barn owl.
During hunting from a perch, barn owls initially turn the head toward
faint sounds (Konishi 1983), apparently waiting for further sounds that might indicate the presence of a potential prey.
This behavior demonstrates that barn owls can draw attention to
particular auditory events. Furthermore localization behavior is
elicited only by specific sounds, indicating that barn owls use
selective attention to assess the relevance of a sound source (Wagner 1995
).
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METHODS |
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Experiments were carried out with two barn owls (Tyto alba) obtained from the institute's breeding colony. Because barn owls are typically active during evening and night, training sessions started within 2 h after dusk. All procedures were approved by the Animal Care Committee of the RWTH Aachen and the Regierungspräsidium Köln.
Owl handling
Before the experiments owls were fixed in the aviary to a perch with leather bands that were permanently bound to their legs. On this perch, owls were carried to the laboratory and placed into the center of the behavioral apparatus. Otherwise they were unrestrained and could make head, body, or wing movements. However, with respect to their main hunting strategy, owls mostly sat upright on the perch and gazed to frontal directions, waiting for relevant stimuli. Two infrared-sensitive video cameras were installed to monitor the owls' general behavior during the experiments.
Stimulus design
The behavioral setup (Fig. 1A) was mounted in an anechoic chamber (IAC, base: 2 × 2 m, height: 2.6 m) that was darkened during the measurements. A custom-built display for the cuing stimulus was placed in front of the owl ~45 cm from the owl's head. The display contained horizontally arranged light-emitting diodes (LEDs), in total covering 5° of visual angle. The number of LEDs was either two (experiment 1) or three (experiment 2, see Experimental design). Acoustic target stimuli were generated by a waveform generator (WG1; all instruments from Tucker Davis Technologies, Gainesville, FL), regulated by an attenuator (PA4), and were randomly switched among four loudspeakers in the owl's periphery (positions: 27 and 47° to the left and right of the owl's midline at 0° elevation, switched by SS1).
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Experimental design
In experiment 1 (Exp. 1), the display for the cuing stimulus consisted of two LEDs. When the owls gazed toward a window of 10° around the center of the display, the cuing stimulus was presented: both LEDs were switched on for 200 ms, then one LED was switched off and the stimulus hemisphere was cued with the remaining LED for another 300 ms. The target sound, a noise burst (100 ms, 50 dB SPL), followed after a variable cue-target delay (200 or 300 ms).
The cue-target delay was always determined as the time elapsing between the offset of the remaining LED and the onset of the target sound.
In experiment 2 (Exp. 2), the display for the cuing stimulus consisted of three LEDs, with two lateral LEDs and a central fixation-LED. The fixation-LED extinguished only during reward delivery and served as a reference for orientation toward the display. When owls gazed forward, one lateral LED was switched on for 500 ms. This LED pointed toward the most probable stimulus hemisphere. The auditory target-stimulus was presented after a variable cue-target delay (200-500 ms, 100-ms steps).
In 80% of the trials, cuing stimuli pointed toward the side of the upcoming target stimulus, and in 20%, they pointed toward the opposite side. Cuing stimuli that were spatially consistent with the target side will be referred to as "valid cuing stimuli," the others will be referred to as "invalid cuing stimuli."
The required behavioral response was a head saccade toward the source of the target stimulus. Correct trials were rewarded with small portions of chick meat delivered from a custom-built feeder. Incorrect responses (see following text) were followed by a manually applied correction trial that was omitted from analysis. Correction trials consisted of the only presentation of the target sound from the same source as in the original trial. This was repeated until the bird responded with a head turn toward the sound source, a response for which the bird was rewarded. In nonresponse trials, owls had to wait for 5 s until they could start the next trial. In a correction trial or during waiting periods, the fixation-LED (only in Exp. 2) was continuously switched on.
Head saccades were measured with a magnetic motion-tracking system
(miniBIRD, Ascension Technology, Burlington, VT, 120-Hz sampling frequency) attached to the owl's head during the experiment. Using the motion-tracking technique, the direction of gaze could reliably be determined from the orientation of the head, as eye movements are virtually absent in owls (Steinbach and Mooney
1972).
Data analysis
Only horizontal head movement trajectories, i.e., rotations around the z axis, were analyzed. Turning angles of head saccades were calculated as the maximum of the horizontal trajectory. Additionally, locations of the loudspeakers relative to the orientation of the owl's head were calculated by measuring the head orientation at the onset of the auditory stimulus and subtracting this angle from the absolute stimulus position. Thereby the external coordinate system was transformed into an owl-centered coordinate system.
As response latency, we defined the time elapsing between the onset of the auditory stimulus and the point when the head saccade exceeded a threshold of 8° minimum turning angle. Due to this threshold criterion, latencies were generally prolonged by about 12 ms with respect to the exact start of the head saccade. Response latencies were afterward log-transformed for multivariate statistics.
Head turns were classified into three response types by a computer
algorithm using simple classification attributes: correct responses,
i.e., head turns toward the sound source with a minimum angle of 8°;
incorrect responses, i.e., head turns away from the sound source with a
minimum angle of 8°; and nonresponses, when the head-turning angle
was <8°, or the latency of the head turn >1,300 ms. For correct and
incorrect responses, the maximum head-turning angle, i.e., the
perceived target direction, had to be stable within 2° for 85 ms.
Both response types generally consisted of a single head movement. Head
shakings, which occurred in <6% of the trials, missed the stability
criterion and were omitted from analysis.
To quantify the stability of initial fixation, we calculated the
magnitude and direction of the largest movement in a 200-ms sliding
window during the time prior to target presentation. Detailed analysis
revealed that the owls made only small head movements while waiting for
the target stimulus: in 84% of the trajectories, the movements were
4°. Most of the early movements occurred at onset of the cuing
stimulus when the owls had gazed to frontal directions but not
precisely toward the display. In Exp. 1, movement directions
showed no consistent pattern with respect to the directional information of the cuing stimulus (Fisher's exact test; owl
1: n = 2,066, P = 0.33; owl
2: n = 912, P = 0.73). In
Exp. 2, movement directions differed significantly after
leftward or rightward pointing cuing stimuli (Fisher's exact test;
owl 1: n = 1,852, P < 0.01;
owl 2: n = 1,622, P < 0.01). However, a separate analysis for each direction of the cuing
stimulus showed, that movement biases in only one of four cases
significantly pointed into the direction of the cuing stimulus
(
2 goodness-of-fit test; owl 1 cued
rightward:
2 = 37.4, P < 0.01).
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RESULTS |
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We obtained 4,768 trials from owl 1 (2,494 in
Exp. 1, 2,274 in Exp. 2) and 3,557 trials from
owl 2 (1,442 in Exp. 1, 2,115 in Exp.
2). Owl 1 made correct responses in between 81 and 83% of the trials, depending on experiment, and owl 2 in between
63 and 77%. Multivariate statistics revealed that the behavioral variability between sessions (Wagner 1993) occurred
independent of trial validity. Correct trials were therefore
collapsed across sessions. Incorrect responses (see
METHODS) occurred, depending on owl and experiment,
in between 3 and 9% of the trials and nonresponses in between 8 and
24% of the trials.
A clear effect of the validity of the cuing stimulus was visible in the response latencies (Fig. 1B); this indicates that spatial attention modulates the processing of sound source location in barn owls. In valid trials, mean response latencies were significantly reduced by between 10 and 22% (mean 16%, i.e., 37.4 ms), depending on owl and experiment. A multivariate ANOVA that tested differences in response latencies among owls, experiments, or valid and invalid trials was significant (F7,6452 = 33.2, P < 0.01). Mean response latencies differed significantly between valid and invalid trials (F1,6452 = 42.5, P < 0.01) and between owls (F1,6452 = 105.0, P < 0.01). The effect of trial validity was robust and showed no interaction with owl (F1,6452 = 0.08, P = 0.77) or experiment (F1,6452 = 0.12, P = 0.73). Latencies generally were similar in both experiments (F1,6452 = 0.02, P = 0.89). Nevertheless in owl 1, latencies increased slightly between experiments, whereas in owl 2, latencies slightly decreased, which led to a significant interaction between owl and experiment (F1,6452 = 33.6, P < 0.01, Fig. 1B). We also found that the effect of trial validity did not depend on relative sound source position in both Exps. 1 and 2 (owl 1: F1,3918 = 0.05, P = 0.82, owl 2: F1,2534 = 2.01, P = 0.16).
Generally the proportions of the response types (correct, incorrect,
and nonresponses) were similar in valid and invalid trials. In
owl 1, however, we found a significant increase of incorrect responses after an invalid cuing stimulus (2
test; Exp. 1: n = 2,143,
2 = 13.3, P < 0.01;
Exp. 2: n = 1,999,
2 = 6.8, P < 0.05).
In contrast to response latencies, turning angles of head saccades in
valid trials were generally similar to those in invalid trials (Fig.
2). In owl 2, an ANCOVA
revealed that turning angles differed between relative sound source
positions and between experiments (F7,2533 = 2,393.2, P < 0.01). Interestingly, turning angles did not differ between valid
and invalid trials (F1,2533 = 1.5, P = 0.23), which indicates, that they were not
modulated by spatial attention. This result was similar between
experiments (F7,2533 = 0.159, P = 0.69) and across relative sound source positions (F7,2533 = 0.158, P = 0.69). In owl 1, a more detailed analysis was performed. We
observed that turning angles were not different between valid and
invalid trials for most stimulus positions with the exception of
stimulus positions around 47° in Exp. 2 (Fig. 2C, ANOVA: F1,496 = 13.7, P < 0.01).
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A general observation from previous studies carried out in other
species is the decrease of mean response latency with increasing cue-target delays (rats: Bushnell 1995; monkeys:
Bowman et al. 1993
; humans: Spence and Driver
1996
). We found, however, that the duration of the cue-target
delay had no effect on response latencies or turning angles of head
saccades (Fig. 3). The cue-target delay
varied between 200 and 300 ms (Exp. 1) or between 200 and 500 ms (100-ms steps, Exp. 2). A multivariate ANOVA that
tested differences in response latencies among cue-target delays, owls, and valid or invalid trials was significant
(F15,6451 = 14.8, P < 0.01). These differences occurred between owls
(F1,6451 = 61.8, P < 0.01) and between valid and invalid trials
(F1,6451 = 29.3, P < 0.01) as revealed before (see preceding text). Surprisingly, latencies
did not vary significantly with the variable duration of the cue-target
delay (F3,6451 = 1.49, P = 0.21). The lack of influence did not depend on the
owl (F3,6451 = 2.03, P = 0.11) or on trial validity (F3,6451 = 0.10, P = 0.94). Multivariate ANOVAs performed for
each experiment separately had the same results. Likewise, turning
angles of head saccades did not vary significantly with the duration of
the cue-target delay (ANOVA: F3,6452 = 1.1, P = 0.33).
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DISCUSSION |
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Effects of spatial selective attention on sound localization have
so far exclusively been studied in humans. Experimental guidance of the
attentional focus was achieved in these studies by peripheral auditory
cuing stimuli (Spence and Driver 1997) or indirect
visual cuing stimuli (Spence and Driver 1994
, 1996
). Spatially consistent cuing stimuli, i.e., valid cuing stimuli, reduced
response latencies toward attended stimulus positions compared with
response latencies toward unattended positions. Here we show that in
owls processing time of sound source location was shortened in a
similar way as in humans by presenting a valid cuing stimulus.
The main criticism on studies carried out in the visual system was,
specifically when peripheral cuing stimuli were used, that the validity
effect is possibly not related to shifts of spatial attention but can
be explained by pure stimulus additivity (rats: Bushnell
1995, humans: e.g., Posner et al. 1984
). For the data presented here, this explanation is highly unlikely. First, the
validity effect was long-lasting and still significant after a
cue-target delay of 500 ms. Thus a visual cuing stimulus influenced the
processing of an auditory target even when the cue had disappeared 500 ms before target onset. Direct interaction over a temporal separation
in this range is highly unlikely. The second possibility could be
stimulus additivity in the spatial domain based on direct interaction
in bimodal neurons, e.g., in the owl's midbrain. This could only
happen if the visual and auditory spatial receptive fields of these
neurons are large enough to cover both stimuli, cue and target. The
knowledge about characteristics of audiovisual neurons in the owl's
midbrain, however, do not support this hypothesis. Bimodal neurons in
the optic tectum generally show small visual receptive fields
(10-17°) (Knudsen 1982
) and a very good alignment of
the centers of the visual and auditory receptive fields (Knudsen 1982
). We therefore used cues and targets that should be
sufficiently separated in space (cue: 2.5° lateral, target: at least
27° lateral). Thus a direct stimulation of the same cell from the
visual cue and the auditory target is highly unlikely in our setup.
Importantly, in our experiment, the effect of cue validity was not influenced by the detailed structure of cuing stimulus, which differed considerably between Exp. 1 (target side was indicated by switching off a LED) and Exp. 2 (target side was indicated by switching on a LED). In both experiments, owls were able to use the cuing stimulus to estimate the most probable position of the next upcoming auditory stimulus as observable by the validity effect. This leads us to the conclusion that the mechanisms resulting in a validity effect may be the same in owls and in humans that emerge from spatial attention.
The duration of the cue-target delay, i.e., the waiting period between
the cuing stimulus and the auditory target, did not affect either
latencies or turning angles of head saccades. In a paradigm providing
prestimuli (informative or uninformative), as used here, subjects are
forewarned that the target stimulus will soon be presented. A waiting
period of randomized duration is often introduced to prevent the
subjects from temporal learning. Nevertheless the probability that the
target stimulus will be presented increases with the duration of the
waiting period. As a result, mammalian species (rats: Bushnell
1995; monkey: Bowman et al. 1993
; humans:
Spence and Driver 1996
) show continuously decreasing
response latencies as the cue-target delay increases. This "alerting
effect" (Niemi and Naatanen 1981
) was found to be
unrelated to the orientation of spatial attention, although it
indicates that other types of attention may be engaged by the cuing
stimulus. Barn owls, however, showed no sensitivity to the increasing
probability of a stimulus appearance. The constraints why this was not
an evolutionary strategy for the owl remain to be investigated.
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ACKNOWLEDGMENTS |
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We thank H. Luksch for critical comments on earlier versions of the manuscript and K. Böhning-Gaese for advice on statistical analyses.
This work was supported by the Deutsche Forschungsgemeinschaft (SPP 1001, "Sensomotorische Integration").
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FOOTNOTES |
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Address for reprint requests: B. H. Gaese, Institut für Biologie II, RWTH Aachen, Kopernikusstr. 16, D-52074 Aachen, Germany (E-mail: gaese{at}bio2.rwth-aachen.de).
Received 13 June 2000; accepted in final form 2 November 2000.
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REFERENCES |
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