A precedence effect resolves phantom sound source illusions in the parasitoid fly Ormia ochracea

Abstract

Localizing individual sound sources under reverberant environmental conditions can be a challenge when the original source and its acoustic reflections arrive at the ears simultaneously from different paths that convey ambiguous directional information. The acoustic parasitoid fly Ormia ochracea (Diptera: Tachinidae) relies on a pair of ears exquisitely sensitive to sound direction to localize the 5-kHz tone pulsatile calling song of their host crickets. In nature, flies are expected to encounter a complex sound field with multiple sources and their reflections from acoustic clutter potentially masking temporal information relevant to source recognition and localization. In field experiments, O. ochracea were lured onto a test arena and subjected to small random acoustic asymmetries between 2 simultaneous sources. Most flies successfully localize a single source but some localize a 'phantom' source that is a summed effect of both source locations. Such misdirected phonotaxis can be elicited reliably in laboratory experiments that present symmetric acoustic stimulation. By varying onset delay between 2 sources, we test whether hyperacute directional hearing in O. ochracea can function to exploit small time differences to determine source location. Selective localization depends on both the relative timing and location of competing sources. Flies preferred phonotaxis to a forward source. With small onset disparities within a 10-ms temporal window of attention, flies selectively localize the leading source while the lagging source has minimal influence on orientation. These results demonstrate the precedence effect as a mechanism to overcome phantom source illusions that arise from acoustic reflections or competing sources.

Fig. 1.

Experimental arena for field phonotaxis trials. A lure speaker orientated upwards was positioned at the 8-cm circular start region underneath the arena. Two test speakers (black triangles) orientated horizontally were separated by 90° and positioned behind sound traps (rectangles). A third (silent) trap was placed between the 2 speakers (0° from the start region). Demarcation lines divided the test arena into 3 choice regions: 2 correct choice regions (light gray) and an incorrect choice region (dark gray).

Fig. 2.

Phonotaxis to simultaneous and single sources under field conditions. Direct responses. Percentage of correct responses with direct approach to source one location (blue). Indirect responses. Percentage of correct responses with initial misdirected walking trajectories to a phantom source (0° heading) (green). Incorrect responses. Percentage of unsuccessful phonotaxis (red) with walking trajectories misdirected toward a phantom source location (0° heading). Most flies were able to resolve an individual source while a smaller proportion of flies walked toward a phantom source location.

Fig. 3.

Phonotaxis to simultaneous sources under laboratory conditions. Two synthetic sound sources broadcast synchronously (0-ms onset delay) to produce overlapping chirps (Inset). (A) Average walking trajectory of free-walking flies to sources separated by 90°. (i) Average response (n = 10 flies). (ii) Individual responses of a single representative fly. (B) Average walking response of flies to sources separated by 180°. (i) Average response (n = 9 flies). (ii) Individual responses of a single representative fly. Gray line within individual response plots (ii) indicate average responses. Square symbols (i) and horizontal/vertical projections from symbols indicate the mean and confidence intervals of the location of flies at 0.03-s intervals. Flies responded to simultaneous sources by directing phonotaxis to a phantom source location between broadcasting speakers (≈45° heading in 90° condition, ≈0° heading in 180° condition).

Fig. 4.

Phonotaxis to interdigitated (10 ms onset delay) sources. Two synthetic sound sources broadcast with a 10-ms onset delay to produce interdigitated chirps (Inset). (A) Average walking response of flies (n = 10 flies) to sources separated by 90°. (B) Average walking response of flies to sources separated by 180° (n = 10 flies). Square symbols and horizontal/vertical projections from symbols indicate the mean and confidence intervals of the location of flies at 0.03-s intervals. Filled symbols indicate walking responses to forward (A) or left (B) leading sound sources while open symbols indicate walking response to lateral or right leading sound sources. Flies responded to interdigitated sources by directing phonotaxis to a phantom source location between the broadcasting speakers (45° heading in 90° condition, 0° heading in 180° condition) but with a slight bias toward leading sources.

Fig. 5.

Phonotaxis to overlapping sources with small onset time differences (5- and 0.2-ms onset delay). Two synthetic sound sources broadcast with a 5-ms onset delay to produce half-overlapping sound pulses (Inset, A and B), or a 0.2-ms onset delay to produce overlapping stimuli out of phase by 1 cycle of the 5-kHz carrier frequency. (A) Average walking responses (square symbols, 5-ms onset delay; circular symbols, 0.2-ms onset delay) of flies to sources spatially separated by 90° (n = 10 flies). (B) Average walking responses of flies to sources spatially separated by 180° (n = 10 flies). Symbols and horizontal/vertical projections from symbols indicate the mean and confidence intervals of the location of flies at 0.07- (A) and 0.03-s (B) intervals. Filled symbols indicate walking responses to forward (A) or left (B) leading sources while open symbols indicate walking response to lateral (A) or right (B) leading sources. Small onset time differences between sources (0.2 ms) allowed flies to resolve source location ambiguity to the leading source.

Fig. 6.

Phonotaxis to overlapping sources with large onset delays (100 ms, 200 ms, and 500 ms). Two synthetic sound sources broadcast with 100 ms onset delay (half-overlapping pulse train), 200 ms onset delay (continuous pulse train), and 500 ms onset delay (2 distinct chirps separated by 300 ms of silence) (Insets, A and B). (A) Average walking responses of flies (n = 7 flies) to sources spatially separated by 90° with onset delays of 100 ms (black), 200 ms (blue), and 500 ms (red). (B) Average walking responses (n = 7 flies) of flies to sources spatially separated by 180° with onset delays of 100 ms (black), 200 ms (blue), and 500 ms (red). Square symbols and horizontal/vertical projections from symbols indicate the mean and confidence intervals of the location of flies at 0.07-ms (A) and 0.03-s (B) intervals. Filled symbols indicate walking responses to forward (A) or left (B) leading sources while open symbols indicate walking response to lateral (A) or right (B) leading sources. Under all temporal overlaps tested, flies initially turned and walked toward the leading source followed by a secondary turning response to the lagging source. Secondary turning responses were weaker for sources separated by 180°.