Natural soundscapes are composed of numerous biotic and abiotic sound sources (Brumm and Slabbekoorn, 2005; Theunissen and Elie, 2014). Even in the presence of natural noise, auditory systems are adept at detecting, recognizing, and localizing sound sources of interest for animals that rely on hearing to mediate appropriate behavioural decisions (Bee and Micheyl, 2008; Lee et al., 2017). Segregating sounds of interest from noise can be challenging because sound waves from multiple sources combine to form a composite waveform prior to auditory transduction. From this input, coherent representations of various sources are derived from the composite waveform and signals of interest are segregated from other competing sound sources (McDermott, 2009). In humans, this sensory challenge is known as the ‘cocktail party problem’ and it describes difficulties encountered in perceiving speech in noisy social settings (Bregman, 1990; Bronkhorst, 2000; Brumm and Slabbekoorn, 2005; Cherry, 1953; Hulse, 2002; McDermott, 2009).

Non-human animals may encounter analogous situations in natural acoustic environments (Bee, 2012; Bee and Micheyl, 2008; Hulse, 2002; Römer, 2013). Some insect choruses are known to produce sustained levels of background noise (Gerhardt and Huber, 2002; Römer, 2013). These choruses are often composed of mixed species with communication signals that may share spectral, temporal, and spatial overlap. Such background noises have the potential to negatively impact the performance of auditory systems in perceiving relevant signals (Brumm, 2013; Brumm and Slabbekoorn, 2005; Wiley, 2015).

Hearing with two ears provides important computational advantages for sound localization and sound source segregation (Schnupp and Carr, 2009). When two ears are spatially separated, each will experience different sound arrival times and sound pressure levels in response to an incident sound wave. Interaural time and level differences (ITD and ILD respectively) are binaural cues that the auditory system can utilize to compute sound direction (Knudsen and Konishi, 1979; Michelsen, 1998). Spatially separated sound sources will give rise to different ITDs and ILDs for each source and sound diffraction between the two ears can generate different signal-to-noise ratios associated with each source leading to a ‘better ear advantage’ for detecting a particular sound source (Blauert, 1997). Both these auditory cues may contribute to spatial release from masking (SRM), a sensory mechanism that allows for improved reception of target signals that are spatially separated from noise sources (Bee and Micheyl, 2008).

Spatial release from masking has been documented in ears that function as independent pressure receivers and in ears that are internally (acoustically) coupled to function as pressure difference receivers (Bee, 2007; Bee and Christensen-Dalsgaard, 2016; Brunnhofer et al., 2016; Caldwell et al., 2016; Dent et al., 1997; Hine et al., 1994; Nityananda and Bee, 2012; Saberi et al., 1991; Schwartz and Gerhardt, 1989; Sümer et al., 2009; Ward et al., 2013). Whether spatial release from masking may contribute to sound source segregation in mechanically coupled pressure receivers remains unknown. Mechanically coupled ears have been described in some tachinid and sarcophagid flies that rely on directional hearing to localize the advertisement signals of suitable host species (Allen, 1995; Cade, 1975; Lakes-Harlan et al., 1999; Robert et al., 1999). Upon source localization, larvae are deposited and develop as parasites within hosts (Adamo et al., 1995; Allen et al., 1999; Cade, 1975).

The ability of Ormia ochracea (Diptera: Tachinidae) to localize cricket calling songs is remarkable because their small physical size severely limits conventional acoustic cues for sound localization (Michelsen, 1998; Robert, 2005). With bilaterally symmetric ears that are separated by a mere 500 µm (Robert et al., 1996a), diffraction of the ~7 cm wavelength field cricket calling song is insufficient to result in measurable acoustic ILDs and the best possible ITD is 1.45 µs for a sound source at 90˚ relative to the midline (Robert et al., 1996b). Despite these minuscule sound field directional cues, O. ochracea are still capable of localizing sound sources to the accuracy of 2˚ azimuth (Mason et al., 2001). This hyperacute directionality is made possible by the mechanical coupling of the two tympana with a flexible cuticular lever that amplifies the sound field ITDs into larger mechanical ITD and ILDs sufficient for neural processing (Oshinsky and Hoy, 2002). The surprising acuity of directional hearing in O. ochracea has led to considerable interest in mechanically coupled auditory systems as models for novel acoustic technology (e.g. Bauer et al., 2016; Kuntzman and Hall, 2014), as well as other applications involving localization of signal sources subject to the so-called ‘aperture problem’ (e.g. Akçakaya and Nehorai, 2010).

In addition to computing sound direction, O. ochracea must also recognize the calling songs of preferred host crickets (Gray et al., 2007). Field cricket calling songs consist of tonal sound pulses with a dominant frequency of about 5 kHz that are repeated at a species-specific pulse rate (Walker, 1962). After song detection, O. ochracea engage in flying (Müller and Robert, 2001) and/or walking phonotaxis to the source (Lee et al., 2009; Mason et al., 2005). Success in localizing host crickets requires the auditory system to integrate two types of temporal information. The auditory system must measure a difference in the timing of sound pulses that arrive at the two ears to determine sound direction, and the timing between consecutive sound pulses for song pattern recognition (species recognition). In this study, we examine whether spatial release from masking may contribute to improved host song recognition and localization in the presence of masking noise. We exploit the directional characteristics of the mechanically coupled tympana and use a point-source band-limited noise to asymmetrically interfere with the temporal pattern input to both sides of the auditory system. If spatial release from masking confers hearing advantages in O. ochracea, behavioural response thresholds are expected to decrease while localization accuracy is expected to increase when noise is spatially separated from a signal of interest (relative to noise and signal sources in close proximity). However, over a range of spatial separations between a target signal and masker (from 6° to 90° of spatial separation), we find no support for SRM in auditory responses of O. ochracea. Rather, a localized masker interferes with auditory directionality, and this effect is more severe for a larger spatial separation between the target signal and masker.

In behavioural experiments, we used a spherical treadmill system (Lott et al., 2007; Mason et al., 2001) to measure walking phonotaxis to a frontal target signal (attractive synthetic cricket trill) and a laterally positioned masker (band-limited noise) (Figure 1A). Test stimuli consisted of a 76 dB SPL 4 s burst of band-limited masker in combination with a 2 s target signal broadcast at different intensities to result in varied signal-to-noise ratios (SNRs) (Figure 1B). Test stimulus presentation started with the broadcast of the masker. The target signal was presented 1 s after the onset of the masker such that the target signal was embedded in the masker.

Figure 1

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Walking responses to the target signal and masker in isolation

Flies remained quiescent in the absence of stimulus presentation. When presented with the standard 76 dB SPL 2 s cricket song from 0° azimuth (Figure 1A) flies responded with a latency of 56.45 ± 2.76 ms after stimulus onset; forward velocity increased to a sustained level of 6.03 ± 0.28 cm/s (Figure 2A) while steering velocity fluctuated around 0 cm/s (Figure 2B). Flies exhibited sustained walking with an angular heading of 2.93 ± 5.25° and covered a total distance of 16.91 ± 0.91 cm (Figure 2C). When subjected to the masker alone from the forward location (0° azimuth) at the same intensity, flies responded with a similar latency of 52.19 ± 3.32 ms (Paired Sample T-Test: n = 13 flies t = 0.741, p = 0.477). After masker onset, forward velocity increased transiently to levels less than those observed in response to the target signal, but rapidly declined to near baseline levels (Figure 2A). Steering velocity appeared to fluctuate more sporadically around 0 cm/s (Figure 2B) as flies responded with a different mean angular heading of 0.76 ± 4.03° (Watson U² Test: n = 13, U² = 0.256, p = 0.01). Although walking responses were directed toward the masker location, responses were short-lived and thus flies traveled a significantly shorter total distance of 2.08 ± 1.01 cm (Paired Sample T-Test: n = 13 flies, t = 9.983, p < 0.001, Figure 2C). Flies did not perform negative phonotaxis (away from the masker) in response to the masker in isolation.

Figure 2

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Figure 2—source data 1

Translational velocity in response to the target signal and masker presented in isolation.

Masker presentation started and ended 0.5 and 4.5 s after the onset of data acquisition, respectively. Signal presentation started and ended 1.0 and 4.0 s after the onset of data acquisition, respectively. Data plotted in Figure 2A.

https://doi.org/10.7554/eLife.20731.004

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Figure 2—source data 2

Steering velocity in response to the target signal and masker presented in isolation.

Masker presentation started and ended 0.5 and 4.5 s after the onset of data acquisition, respectively. Signal presentation started and ended 1.0 and 4.0 s after the onset of data acquisition, respectively. Data plotted in Figure 2B.

https://doi.org/10.7554/eLife.20731.005

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Figure 2—source data 3

Virtual walking path in response to the target signal and masker presented in isolation.

‘X’ and ‘Y’ coordinates of virtual walking paths measured from the treadmill system. Data plotted in Figure 2C.

https://doi.org/10.7554/eLife.20731.006

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Increased spatial separation does not decrease masked behavioural response thresholds

We estimated behavioural response thresholds using an approached described in Bee and Schwartz (2009). Behavioural response thresholds depended on the masking condition (Repeated Measures ANOVA: F_{(1.12, 12.33)} = 72.36, p < 0.001, Figure 3). In quiet, flies responded with phonotaxis to the target signal at a mean threshold intensity of 50.80 ± 5.44 dB SPL. Adding a masker that was spatially separated by 6° from the frontal signal (small separation) significantly increased response thresholds to 63.31 ± 2.64 dB SPL (F_{(1, 11)} = 66.39, p < 0.001). Increasing the spatial separation from 6° to 90° (large separation) between the target signal and masker resulted in a mean response threshold of 63.19 ± 2.96 dB SPL that did not differ significantly from response thresholds when the signal and masker was separated by 6° (F_{(1, 11)} = 0.07, p = 0.80).

Figure 3

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Figure 3—source data 1

Behavioral response thresholds to a target signal in quiet, and signal and masker separated by 6° or 90°.

Data plotted in figure.

https://doi.org/10.7554/eLife.20731.008

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Effects of SNR and source separation on sound localization

Response latencies for the target signal were not significantly affected by SNR (Repeated Measures ANOVA: F_(2,12) = 0.412, p = 0.671) or source separation (F_(1,6) = 0.001, p = 0.974). Flies responded with an average latency of 59.51 ± 3.51 ms. Total distance travelled did not depend on source separation (F_(1,9) = 0.092, p = 0.768) but was significantly affected by SNR (F_(2,18) = 8.601, p = 0.002). A linear contrast revealed that walking distance increased with SNR (linear contrast: F_(1,9) = 15.456, p = 0.03). With an increase in SNR from −6 dB to +6 dB, walking distance increased from 11.35 ± 1.81 cm to 16.36 ± 1.12 cm. Post Hoc contrasts revealed that a SNR of −6 dB resulted in significantly shorter distances walked than at higher SNRs (−6 dB vs 0 dB SNR: F_{(1, 1)} = 8.466, p = 0.017; −6 dB vs +6 dB SNR: F_{(1, 1)} = 15.456, p = 0.003).

Forward velocity profiles reveal a strong but brief walking component in response to the masker that quickly decayed before song onset (Figure 4A). During song presentation, forward velocity increased as a function of SNR (Repeated Measures ANOVA: F_(2,14) = 25.381, p < 0.001) but not song and masker separation (F_(1,7) = 1.866, p = 0.214). With an increase in SNR from −6 dB to +6 dB SNR, average forward velocity increased from 2.26 ± 0.46 cm/s to 4.67 ± 0.39 cm/s but all were significantly less than the average forward velocity of 6.03 ± 0.28 cm/s in response to the song in isolation (Control vs. −6 dB SNR: F_(1,9) = 56.86, p < 0.001, Control vs. 0 dB SNR: F_(1,9) = 46.79, p < 0.001, Control vs.+6 dB SNR: F_(1,9) = 26.24, p = 0.001). SNR-dependent changes in forward velocity corresponded with SNR-dependent changes in walking distances (above).

Figure 4

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Figure 4—source data 1

Translational velocity in response to a target signal and masker separated by 6° and presented at different signal-to-noise ratios (SNRs).

The target signal was presented at 76 dB SPL while the masker intensity was varied to achieve three SNRs (−6, 0, +6 dB). Masker presentation started and ended 0.5 and 4.5 s after the onset of data acquisition, respectively. Signal presentation started and ended 1.0 and 4.0 s after the onset of data acquisition, respectively. Data plotted in Figure 4A (left).

https://doi.org/10.7554/eLife.20731.010

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Figure 4—source data 2

Steering velocity in response to a target signal and masker separated by 6° and presented at different signal-to-noise ratios (SNRs).

The target signal was presented at 76 dB SPL while the masker intensity was varied to achieve three SNRs (−6, 0, +6 dB). Masker presentation started and ended 0.5 and 4.5 s after the onset of data acquisition, respectively. Signal presentation started and ended 1.0 and 4.0 s after the onset of data acquisition, respectively. Data plotted in Figure 4B (left).

https://doi.org/10.7554/eLife.20731.011

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Figure 4—source data 3

Virtual walking path in response to a target signal and masker separated by 6° and presented at different signal-to-noise ratios (SNRs).

The target signal was presented at 76 dB SPL while the masker intensity was varied to achieve three SNRs (−6, 0, +6 dB). ‘X’ and ‘Y’ coordinates of virtual walking paths measured from the treadmill system. Data plotted in Figure 4C (left).

https://doi.org/10.7554/eLife.20731.012

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Figure 4—source data 4

Translational velocity in response to a target signal and masker separated by 90° and presented at different signal-to-noise ratios (SNRs).

The target signal was presented at 76 dB SPL while the masker intensity was varied to achieve three SNRs (−6, 0, +6 dB). Masker presentation started and ended 0.5 and 4.5 s after the onset of data acquisition respectively. Signal presentation started and ended 1.0 and 4.0 s after the onset of data acquisition, respectively. Data plotted in Figure 4A (right).

https://doi.org/10.7554/eLife.20731.013

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Figure 4—source data 5

Steering velocity in response to a target signal and masker separated by 90° and presented at different signal-to-noise ratios (SNRs).

The target signal was presented at 76 dB SPL while the masker intensity was varied to achieve three SNRs (−6, 0, +6 dB). Masker presentation started and ended 0.5 and 4.5 s after the onset of data acquisition respectively. Signal presentation started and ended 1.0 and 4.0 s after the onset of data acquisition, respectively. Data plotted in Figure 4B (right).

https://doi.org/10.7554/eLife.20731.014

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Figure 4—source data 6

Virtual walking path in response to a target signal and masker separated by 90° and presented at different signal-to-noise ratios (SNRs).

The target signal was presented at 76 dB SPL while the masker intensity was varied to achieve three SNRs (−6, 0, +6 dB). ‘X’ and ‘Y’ coordinates of virtual walking paths measured from the treadmill system. Data plotted in Figure 4C (right).

https://doi.org/10.7554/eLife.20731.015

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At the onset of the masker, flies initiated small, transient steering responses toward the masker (negative velocities) with durations that depended on masker intensity (F_(2,14) = 7.804, p = 0.05, Figure 4B) but not location (F_(1,7) = 1.828, p = 0.218, Figure 4B). Steering toward the masker lasted between 65.00 ± 20.44 ms and 157.01 ± 29.59 ms as masker intensity was dropped from 82 dB to 70 dB SPL. This was followed by a quick transition to steering away from the masker.

Overall walking direction (angular heading) depended on the spatial separation between the signal and masker (Two-way Circular ANOVA (hk test): n = 13, F_(1,65) = 8.0324, p = 0.0061, Figure 4C), but not SNR (F_(2,65) = 1.2105, p = 0.3047), or the interaction between source separation and SNR (F_(2,65) = 0.7298, p = 0.4859). In response to the simultaneous broadcast of the target signal and masker from speakers separated by 6° (small separation), there was a slight tendency for flies to deviate further from the control direction with greater directional variability at the lowest SNRs. With a short latency after the onset of signal presentation, flies steered away from the masker with an overall average velocity of 0.37 ± 0.15 cm/s that did not significantly change to different SNRs (F_(2,14) = 1.115, p = 0.355, Figure 4B). Flies responded with similar angular headings (−6 dB: −10.19 ± 14.99°, 0 dB: −4.85 ± 7.41°, +6 dB: −5.69 ± 4.41°) for all SNR treatments and these differed significantly from controls (2.93 ± 5.25°) (Hotelling’s Pair-Sample Test: control vs. −6 dB SNR, n = 11, F = 5.7276, p = 0.0249; control vs. equal dB SNR, n = 13, F = 7.0532, p = 0.0107, control vs. +6 dB SNR, n = 13, F = 14.1137, p = 0.0012, Figure 4C).

In response to the simultaneous broadcast of target signal and masker separated by 90° (large separation), flies oriented to different mean angular headings at different SNRs (−6 dB: −15.02 ± 7.42°, 0 dB: −12.75 ± 3.75°, +6 dB: −10.39 ± 2.19°), all of which were significantly different from responses to controls (control vs. −6 dB SNR, n = 13 F = 6.6895, p = 0.0238; control vs. equal dB SNR, n = 13, F = 37.8136, p < 0.0001, control vs. +6 dB SNR, n = 13, F = 43.6432, p < 0.0001, Figure 4C). At −6 dB SNR, angular heading did not differ for the two source separations (−6 dB SNR 6° vs. 90°: F = 0.7372, n = 13, p = 0.5173). However, signal and masker separation caused a significant shift contralateral to the location of the masker for 0 dB and +6 dB SNR respectively (0 dB SNR 6° vs. 90° separation: F = 7.0648, n = 13, p = 0.0106, +6 dB SNR 6° vs. 90° separation: F = 3.9304, n = 13, p = 0.055, Figure 4C). Steering velocity depended on source separation (F_(1,7) = 9.193, p = 0.019, Figure 4B). When the signal and masker were separated by 90°, steering velocity increased to 1.07 ± 0.34 cm/s and movement was directed away from the target signal and masker (Figure 4C).

Effects of balanced temporal pattern interference on localization accuracy

Additional behavioural experiments were conducted to establish whether binaurally balanced noise would restore accurate signal localization. In these experiments, we equalized temporal pattern interference with a second coherent (identical) masker positioned at a location that is a direct mirror reflection of the other masker location (Figure 1A). When the signal was presented in isolation, flies walked a total distance of 7.74 ± 0.45 cm and localized a frontal 76 dB SPL signal with an angular heading of −0.32 ± 3.1° (Figure 5A). When the masker was broadcast along with the target signal at equal intensity and spatially separated by 6° to the right (Figure 5B) or left (Figure 5C) of the target signal speaker, flies responded with mean angular headings contralateral to the masker location (right masker: −13.46 ± 7.95°, left masker: 11.46 ± 7.80°). When the signal and masker were separated by 90° (Figure 5E,F) flies responded with significantly different mean angular headings (6° vs. 90° separation right masker: n = 12, U² = 0.51, p < 0.001, 6° vs. 90° separation left masker: n = 12, U² = 0.51, p < 0.001) that were diverted further away from the signal location (right masker: −47.04 ± 11.91°, left masker: 46.93 ± 16.08°). With a second identical masker, regardless of whether the signal and masker were separated by 6° (Figure 5D) or 90° (Figure 5G), flies consistently walked less (F_(1,11) = 4.209, p = 0.04) and localized a forward direction (6° separation: 1.93 ± 3.35°, 90° separation: 2.82 ± 6.19°) that did not differ from responses to a forward target signal in quiet (signal alone vs. maskers with a 6° separation: n = 12, U² = 0.05, p > 0.5, signal alone vs. maskers with a 90° separation: n = 12, U² = 0.12, p > 0.1).

Figure 5

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Figure 5—source data 1

Virtual walking path in response to the target signal presented in isolation.

The target signal was presented at 76 dB SPL from a forward speaker. ‘X’ and ‘Y’ coordinates of virtual walking paths measured from the treadmill system. Data plotted in Figure 5A.

https://doi.org/10.7554/eLife.20731.017

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Figure 5—source data 2

Virtual walking path in response to a target signal and masker (on the right) separated by 6° and presented at equal intensity.

The target signal was presented at 76 dB SPL from a forward speaker while the masker was presented at the same intensity from an adjacent speaker to the right. ‘X’ and ‘Y’ coordinates of virtual walking paths measured from the treadmill system. Data plotted in Figure 5B.

https://doi.org/10.7554/eLife.20731.018

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Figure 5—source data 3

Virtual walking path in response to a target signal and masker (on the left) separated by 6° and presented at equal intensity.

The target signal was presented at 76 dB SPL from a forward speaker while the masker was presented at the same intensity from an adjacent speaker to the left. ‘X’ and ‘Y’ coordinates of virtual walking paths measured from the treadmill system. Data plotted in Figure 5C.

https://doi.org/10.7554/eLife.20731.019

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Figure 5—source data 4

Virtual walking path in response to a target signal and maskers separated by 6° and presented at equal intensity.

The target signal was presented at 76 dB SPL from a forward speaker while two coherent maskers were presented at the same combined intensity from adjacent speakers to the left and right of the signal speaker. ‘X’ and ‘Y’ coordinates of virtual walking paths measured from the treadmill system. Data plotted in Figure 5D.

https://doi.org/10.7554/eLife.20731.020

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Figure 5—source data 5

Virtual walking path in response to a target signal and masker (on the right) separated by 90° and presented at equal intensity.

The target signal was presented at 76 dB SPL from a forward speaker while the masker was presented at the same intensity from a lateral speaker to the right. ‘X’ and ‘Y’ coordinates of virtual walking paths measured from the treadmill system. Data plotted in Figure 5E.

https://doi.org/10.7554/eLife.20731.021

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Figure 5—source data 6

Virtual walking path in response to a target signal and masker (on the left) separated by 90° and presented at equal intensity.

The target signal was presented at 76 dB SPL from a forward speaker while the masker was presented at the same intensity from a lateral speaker to the left. ‘X’ and ‘Y’ coordinates of virtual walking paths measured from the treadmill system. Data plotted in Figure 5F.

https://doi.org/10.7554/eLife.20731.022

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Figure 5—source data 7

Virtual walking path in response to target signal and maskers that are separated by 90° and presented at equal intensity.

The target signal was presented at 76 dB SPL from a forward speaker while two coherent maskers were presented at the same combined intensity from lateral speakers to the left and right of the signal speaker. ‘X’ and ‘Y’ coordinates of virtual walking paths measured from the treadmill system. Data plotted in Figure 5G.

https://doi.org/10.7554/eLife.20731.023

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Tympanal measurements

We hypothesized that these results could be explained by the interaction of an asymmetrically placed masker with the directional properties of O. ochracea’s peripheral auditory system, which would differentially bias the perceived SNR at each ear. Because the masker-ipsilateral ear would show a stronger masker-driven response than the contralateral, whereas the signal-driven responses of the two ears would be equal. We refer to this ear-specific SNR as the effective amplitude of responses (i.e. response to target signal above the response to masker) to avoid confusion with the SNR of the broadcast stimulus, which we manipulated in our experiments (Figure 6A). The overall effect of such a bias in effective response amplitude would be to mimic binaural cues for a lateral signal source location (Figure 9). We verified that this was the case by recording tympanal vibrations with a laser Doppler vibrometer (LDV). We recorded tympanal responses for repeated presentations of a target signal and masker separated by 6° or 90°, matching speaker configurations in behavioural experiments (Figure 6). Both tympana vibrate at the onset of the masker and continued to do so throughout masker presentation. Vibration amplitudes were elevated during target signal presentation. When the signal and masker were separated by 6°, the effective amplitude was only slightly larger in the masker-contralateral ear compared to the masker-ipsilateral ear (Figure 6B,D). When the spatial separation between the target signal and masker was increased to 90°, there was a pronounced increase in effective amplitude measured from the masker-contralateral ear (Figure 6C,D).

Figure 6

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Figure 6—source data 1

Raw traces of tympanal vibration in response to combined signal and masker under conditions of masker source located near (separated by 6°) or far (separated by 90°) from signal source.

Ipsi- and contralateral refer to the masker. Signal pulses were repeated at 400 ms intervals during continuous masker broadcast.

https://doi.org/10.7554/eLife.20731.025

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Figure 6—source data 2

Normalized-amplitude tympanal vibration responses.

Vibration measurements are normalized to the peak response in response to the target signal. Data plotted in Figure 6B,C.

https://doi.org/10.7554/eLife.20731.026

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Figure 6—source data 3

Smoothed tympanal vibration responses.

Measurements smoothed with a 2000-point sliding rms window.

https://doi.org/10.7554/eLife.20731.027

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Figure 6—source data 4

Effective amplitude measurements.

Effective amplitude measurements (i.e. within-trace signal-to-noise ratio) from smoothed tympanal responses for 23 iterations of signal within the masker. Signal amplitudes were measured from 30 ms time segments corresponding with signal pulses; masker amplitudes were measured from 30 ms segments in the middle of the interpulse interval (i.e. 200 ms after signal-pulse onset). Data plotted in Figure 6D.

https://doi.org/10.7554/eLife.20731.028

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To quantify this effect, tympanal vibrations were recorded in response to a range of broadcast SNRs when the target signal and masker were separated by 90°. Effective response amplitude depended on the SNR (Repeated Measures ANOVA: n = 6, F_{(1.08, 5.41)} = 34.13, p = 0.001) and masker location (F_{(1, 5)} = 14.44, p = 0.013), but not the interaction between SNR and masker location (F_{(1.10, 5.46)} = 2.46, p = 0.173). The effective amplitude increased with increasing SNR and was greater for the masker-contralateral tympanum across all SNRs (Figure 7A).

Figure 7

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We determined the 'effective' interaural vibration amplitude difference (IVAD) as a difference in the effective response amplitude between the ears. We applied our IVAD measurements and previously published tympanal directionality data (Robert et al., 1996b) to generate predictions of the apparent incident sound direction for the target signal embedded in the masker (Figure 7B). Predicted incident sound directions closely matched mean angular headings measured in behavioural experiments across all SNRs (Figure 7C). For example, at equal SNR (0 dB), the interaural effective amplitude difference was measured to be −2.76 ± 0.54 dB which translates to a predicted incident sound direction of −15.10 ± 5.16°. At this SNR, flies localized a sound direction of −12.75 ± 3.75° and this did not differ significantly from the predicted incident sound direction of the target signal (Watson-Williams F-test: F = 0.17, p = 0.69).

A SNR of −6 dB resulted in an interaural effective amplitude difference of 1.71 ± 0.75 dB and a predicted incident sound direction of 10.85 ± 6.79°. A mean interaural effective amplitude of 2.76 ± 0.54 dB was measured for a SNR of 0 dB and this corresponds to an incident sound direction of 15.10 ± 5.16°. When the SNR was increased to +6 dB, this resulted in a measured interaural effective amplitude difference of 2.35 ± 0.66 dB and a predicted sound direction of 13.48 ± 6.39°. These apparent incident sound directions, predicted by effective response amplitude differences, closely matched actual angular headings in behavioural responses (see above) (all p-values > 0.05).

Neural measurements

To determine if peripheral neural responses support the hypothesis that the salience of auditory stimuli is determined by the effective amplitude, we made multi-unit recordings from the left and right frontal (auditory) nerve simultaneously in response to the target signal and masker separated by 90° (Figure 8A). We applied signal detection theory to determine the masker level at which masking occurred for the frontal target signal masked by an ipsilateral or contralateral masker (Figure 8B). In quiet, auditory-evoked impulses were stereotypically timed with the occurrence of the pulse pattern (target signal) (Figure 8A). As masker intensity was increased, acoustically evoked impulses occurred at the onset of the masker and continued to occur randomly in time throughout masker presentation. Target signal-driven activity was readily discernible at high SNR, but became obscured by masker-driven activity at lower SNRs (greater masker levels). The SNR at which target-signal driven activity was masked was lower for the masker-contralateral ear compared to the masker-ipsilateral ear (Figure 8A). For the masker-contralateral ear, signal detection occurred up to a masker level of 66.75 ± 0.73 dB. However, signal detection from the masker-ipsilateral ear was limited to a significantly lower masker level of 59.66 ± 0.58 dB (Paired T-Test: n = 10, t = 7.562, p < 0.001) (Figure 8C). In other words, target signal detection was possible at a much higher masker level for the masker-contralateral ear compared to the masker-ipsilateral ear. Thus, the masker-contralateral ear was most sensitive to target signal detection.

Figure 8

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Figure 8—source data 1

Root Mean Square (RMS) values calculated from multiunit recordings of left and right auditory nerve.

RMS calculated over 40 ms time segments during an interval with a target signal and masker separated by 90° and broadcast at varied signal-to-noise ratios (−18, –12, −6, 0, +6 dB), and an equivalent time window during masker broadcast alone. Signal detection theory was applied to RMS measurements to determine masked thresholds for the masker ipsi- and contralateral ears. These data are plotted in Figure 8C.

https://doi.org/10.7554/eLife.20731.031

Download elife-20731-fig8-data1-v4.xlsx

Ormia ochracea responded with greater walking distances, consistent response latencies, and localized the target signal with improved accuracy in the absence of a masker. Broadcasting the masker over the target signal increased response thresholds and compromised the ability of flies to resolve signal location at all SNRs. Changes in SNR altered walking distance, and to a lesser extent, walking direction. However, increasing the spatial separation from 6° (small separation) to 90° (large separation) between the target signal and masker did not improve signal localization or decrease behavioural response thresholds, but caused flies to divert their walking responses even further away from both sources. More interestingly, the direction of diverted walking was not random, but depended on the masker location.

Beyond demonstrating the potential lack of SRM in O. ochracea, our goals were to show how spatial separation between a target signal and masker affects localization responses, and peripheral sensory mechanisms that may account for localization behaviour. In experiments that test for SRM, a masker can be presented from a forward location while a target signal is displaced relative to the masker (Caldwell et al., 2016; Holt and Schusterman, 2007). Similar to some previous studies that have successfully shown SRM, we chose to present a target signal from a fixed forward direction while a masker was displaced relative to the target signal (Dent et al., 2009; Litovsky, 2005; Turnbull, 1994). This target signal location allowed us to easily assess the accuracy of sound localization (i.e. localization to 0° azimuth in response to a forward target signal). Several response characteristics of open-loop walking phonotaxis in O. ochracea would render assessment of localization accuracy difficult when a target signal is displaced relative to a forward masker. Under open-loop tethered walking phonotaxis, O. ochracea receive no corrective sensory feedback when orienting on the treadmill. As a result, turns toward a lateral target signal location tend to overshoot actual source azimuth (Mason et al., 2005). Furthermore, O. ochracea exhibit graded turning responses that vary with sound direction, but saturate for sound presentation angles greater than ±30° azimuth (Mason et al., 2001). Both of these considerations would make it problematic to quantify the accuracy of phonotaxis, since the predicted orientation is only clearly defined for a forward-located source.

Diverted walking responses appear to be driven by directional response properties of the two tympana that altered the perceived location of the target signal (Lee et al., 2009). For a frontal sound source, both left and right tympana are expected to respond equally in timing and amplitude (Robert et al., 1996b), resulting in equivalent afferent activity on both sides of the auditory system. Under this symmetrical stimulation, flies perceived the target signal location to be straight ahead and responded by phonotaxis to a forward location (Figure 2C). Our laser vibrometry measurements indicate that adding a masker positioned off the midline axis caused the two tympana to vibrate asymmetrically (Figures 6 and 7). The masker-ipsilateral tympanum exhibited a stronger masker-driven response compared to the masker-contralateral tympanum (Figure 7A). Consequently, the masker-contralateral tympanum responded with a lower noise floor that allowed for a greater signal-driven effective amplitude of vibration relative to the masker-ipsilateral tympanum. Neural measurements from the left and right auditory nerve also revealed that target signal detection was possible at higher masker levels for the masker-contralateral ear and thus, resulted in better signal detection (Figure 8). Consistent with our hypothesis, flies orient to a sound-source direction that is a function of the relative effective amplitude between the two tympana and in the direction of the ear with the best signal detection (Figure 9). When a second identical masker was broadcast to equalize masking interference on both sides of the auditory system, symmetry in target signal temporal pattern input was restored and diverted walking responses were corrected so that flies localized the target signal location accurately (Figure 5).

Figure 9

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The nature of auditory coding in O. ochracea suggests that an effect of continuous noise would be to decrease the effective (or perceived) intensity of an attractive stimulus. At the neural level most auditory receptors in O. ochracea are Type I afferents that are phasic and precisely mark the onset of a sound pulse with a single spike followed by a refractory period of approximately 4 ms (Oshinsky and Hoy, 2002). Type II afferents respond similarly but with several spikes at pulse onset (Oshinsky and Hoy, 2002). This is a coding strategy that exploits the predictable, pulsatile pattern of cricket songs by registering the onset timing of successive pulses within a chirp with synchronous bursts of phasic afferent activity. A smaller population of afferents, Type III, are tonic and maintain spiking activity throughout the duration of sound pulses (Oshinsky and Hoy, 2002). Continuous noise is not expected to elicit regular activity in Type I or II afferents (although stochastic amplitude fluctuations in the noise envelope may elicit synchronous afferent spikes). The overall effect, therefore, is to set the noise floor above which a signal-driven increment in vibration amplitude is required to elicit a neural response. For a point-source noise, these effects are greater in the noise-ipsilateral ear and will tend to simulate a directional bias of the song location in the direction of the noise-contralateral ear.

At the onset of the masker, our noise stimulus may have evoked Type 1 afferents to fire similarly to the onset of sound pulses within a cricket song. Thus at the onset of the masker, flies oriented transiently to the masker (Figure 4) but did not sustain walking (Figure 3) in the absence of an attractive temporal pattern. When flies perceived an attractive source over the masker, the strength of phonotaxis increased in a SNR-dependent manner (Figures 3 and 5).

In our experiments, band-limited noise was used to interfere with temporal pattern input. In similar experiments, Wendler (1989) and Stabel et al. (1989) presented a constant tone from an azimuthal location that asymmetrically disrupted temporal pattern input to the cricket auditory system. This resulted in diverted walking responses away from the tone location (Stabel et al., 1989; Wendler, 1989). Neural measurements revealed that the activity of the tone-contralateral auditory interneurons (AN1 and AN2) better represented the song temporal pattern (Stabel et al., 1989). More recent behavioural experiments have shown that song pattern recognition modulates the strength of phonotaxis, while the direction of localization depends on reactive steering to individual sound pulses (Hedwig and Poulet, 2004, 2005; Poulet and Hedwig, 2005). These results suggest that crickets responded to a direction that should balance auditory input. When we introduced a second coherent masker on the opposite side of the auditory system to balance temporal pattern interference, symmetrical auditory input was restored and flies accurately localized the frontal attractive sound source. Our results extend these previous findings to show that the mechanically coupled ears of O. ochracea function as a sensitive bilateral symmetry detector for song temporal pattern. Flies engage in turning responses in attempt to balance temporal pattern input for accurate sound localization.

Animals often experience lower masked thresholds when masking noise is spatially separated from signals of interest (Caird et al., 1989; Dent et al., 1997; Hine et al., 1994; Holt and Schusterman, 2007; Ison and Agrawal, 1998; Schmidt and Römer, 2011; Schwartz and Gerhardt, 1989; Warnecke et al., 2014). SRM necessitates that peripheral directionality will give rise to different interaural cues associated with a target signal and noise that vary as a function of spatial separation (Caldwell et al., 2014). The magnitude of SRM may be further enhanced by central mechanisms (Brunnhofer et al., 2016; Lin and Feng, 2003). Despite peripheral directionality provided by the mechanically coupled ears of O. ochracea, our behavioural threshold measurements provide no evidence of SRM in O. ochracea. Specifically, with increased spatial separations from 6° to 90° azimuth, we did not observe any indication of SRM. This is in stark contrast to some other animals that undoubtedly experience SRM over similar target signal and noise separations (i.e. from 7.5° to 90° separation between a target signal and masker) (Bee, 2007). However, our current results do not exclude the possibility that SRM may occur at smaller azimuthal separations (<6° azimuth). Further experiments that measure behavioural response thresholds to a target signal and masker presented from the same spatial location would address this possibility. Even if SRM occurs at smaller spatial separations, our results would suggest that any SRM in O. ochracea is rather limited and saturates quickly beyond 6° of spatial separation.

We suggest two reasons that may explain this unexpected result. When signal and noise arise from the same spatial location, each ear will experience identical binaural cues (ITD and ILD) from both sources. As signal and noise are spatially separated, differences in these cues associated with each source will occur at both ears. First, the auditory system of O. ochracea may be unable to segregate interaural cues of the target signal from those that are associated with the noise source and this may be one limitation to the function of mechanically coupled ears. SRM does not appear to function in grasshoppers for similar reasons (Ronacher and Hoffmann, 2003). In grasshoppers, directional information and temporal recognition are processed in parallel such that input from both sides of the auditory system are summed internally (von Helversen, 1984; von Helversen and von Helversen, 1995) and thus, binaural cues associated with an attractive signal would be mixed with binaural cues associated with noise. Second, when a point source noise was positioned asymmetrically about the midline axis, flies performed phonotaxis in the direction of the ear with better temporal pattern detection (‘better ear’). The noise source provided directional masking that caused a shift in the perceived location of the target signal location away from the actual source location (Figures 5 and 6) and flies responded by turning in a direction that would balance temporal pattern input. Under more natural conditions (with freely walking flies), this would still allow successful localization of the target (host) source. Initially, misdirected movement would result in a shift of the relative spatial positions of the target and noise sources allowing flies to arrive at the target by an indirect path. Previous work has shown that for multiple competing attractive sources, flies rely on temporal cues for source segregation, via a precedence effect, combined with a preference for forward locations (Lee et al., 2009). We now show that noise can bias the perceived directionality of attractive sources. Future studies will examine how these processes interact to support the surprising spatial hearing abilities of O. ochracea.

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Author details

1. Norman Lee

   Department of Biological Sciences, Integrative Behaviour and Neuroscience Group, University of Toronto Scarborough, Toronto, Canada

   Present address

   Department of Biology, St. Olaf College, Northfield, Minnesota, United States

   Contribution

   NL, Conceptualization, Data curation, Software, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing

   For correspondence

   lee33@stolaf.edu

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0001-6198-710X

2. Andrew C Mason

   Department of Biological Sciences, Integrative Behaviour and Neuroscience Group, University of Toronto Scarborough, Toronto, Canada

   Contribution

   ACM, Conceptualization, Resources, Data curation, Software, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Visualization, Methodology, Writing—original draft

   Competing interests

   The authors declare that no competing interests exist.

   "This ORCID iD identifies the author of this article:" 0000-0001-7719-8500

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