Active listening for spatial orientation in a complex auditory scene

Abstract

To successfully negotiate a complex environment, an animal must control the timing of motor behaviors in coordination with dynamic sensory information. Here, we report on adaptive temporal control of vocal-motor behavior in an echolocating bat, Eptesicus fuscus, as it captured tethered insects close to background vegetation. Recordings of the bat's sonar vocalizations were synchronized with high-speed video images that were used to reconstruct the bat's three-dimensional flight path and the positions of target and vegetation. When the bat encountered the difficult task of taking insects as close as 10-20 cm from the vegetation, its behavior changed significantly from that under open room conditions. Its success rate decreased by about 50%, its time to initiate interception increased by a factor of ten, and its high repetition rate "terminal buzz" decreased in duration by a factor of three. Under all conditions, the bat produced prominent sonar "strobe groups," clusters of echolocation pulses with stable intervals. In the final stages of insect capture, the bat produced strobe groups at a higher incidence when the insect was positioned near clutter. Strobe groups occurred at all phases of the wingbeat (and inferred respiration) cycle, challenging the hypothesis of strict synchronization between respiration and sound production in echolocating bats. The results of this study provide a clear demonstration of temporal vocal-motor control that directly impacts the signals used for perception.

Figure 1. Schematic of Flight Room

Shows setup for video and sound recordings of flight path and acoustic behavior of bats (b) capturing tethered mealworms (w) close to an echo clutter-producing plant (p). Two high-speed video cameras (c1 and c2) were mounted in the room to permit 3-D reconstruction of the bat's flight path in the calibrated space (c.s.). Video recordings were synchronized with audio recordings taken with ultrasonic microphones (m1 and m2) placed on the floor delivering signals to a digital acquisition system (IOtech WaveBook).

Figure 2. Bat Performance

Percentage of attempts and successful captures increased as the target–clutter separation increased, whereas the percentage of trials in which animals made no attempt to capture the target decreased. The bats' performance was tested in 51, 63, 70, and 32 trials at clutter distances of 10, 20, and 40 cm and open room, respectively.

Figure 3. Average Trial Time

The trial duration decreased with increasing target–clutter separation to the shortest duration for open room, measured in 11, 27, 36, and 31 trials at 10-, 20-, and 40-cm clutter distance and open room, respectively.

Figure 4. Bat Flight Paths

Shows plots of the bat flight paths and vocal temporal patterns recorded from three selected trials run with target–clutter separations of 10, 20, and 40 cm and open room. The far-left side shows 3-D plots of the bat's flight path with respect to the plant. The direction of the bat's approach is indicated by an arrow. The middle section shows overhead perspectives on the same four trials. Positions of branches are indicated by green asterisks and position of the worm is indicated by blue circles. The segment of the flight path shown in red corresponds to the time period in which the bat produced strobe groups. Again, arrows indicate the direction of the bat's flight path. The far-right side plots PIs of the sonar signals recorded during the approach and terminal phases of insect pursuit in each trial. Note that the example at 10 cm shows no buzz, as this was an aborted trial. In the open room example, the bat produced strobe groups as it first flew close to the target, but not in the final approach and interception of the target. Each of these examples shows a decrease in PI as the bat approaches the target and clear examples of sonar strobe groups. The strobe groups are characterized by stable PIs (up to 5% variation about the mean PI), interrupted by breaks that are at least 1.2 times the mean PI. The strobe groups produced by the bat in each of these examples are circled in the PI plots. In many instances, the production of strobe groups occurs over hundreds of milliseconds.

Figure 5. Time Waveforms and Spectrograms

Displays time waveforms and spectrograms of the sounds produced in the four trials presented in Figure 4 for 10-, 20-, and 40-cm clutter separation and open room. The left side plots the time waveforms from approximately 2.5 s before target contact to 0.5 s after target contact. The shaded regions display the portion of each trial that is presented in the PI plots of Figure 4, starting at 1.5 s before the time of target contact. Spectrograms of the trial segment shaded in gray are presented in Figure 5 on the right side. The sounds that are defined as belonging to sonar strobe groups are identified with open red circles marked along the time axis below the spectrograms. Along this time axis, blue filled circles mark the occurrence of all other sounds.

Figure 6. Control over Timing of Pulse Emission

(A) shows the timing of sounds from a selected trial and the relation of the sonar strobe groups to the bat's wingbeat cycle, measured from the high-speed video recordings and illustrates that the coupling to wingbeat rate is not strict. (B) plots the distribution of sounds during the upstroke (exhalation; shown in blue) and downstroke (inhalation; shown in red) of the bat's wingbeat for sounds with different PIs, over nine trials. The total number of vocalizations included in the 10-ms PI time bins increases with decreasing PI, because the bat increases the number of vocalizations at shorter intervals as it approaches the target. Note that the distribution of sounds produced during the upstroke and downstroke of the wingbeat cycle becomes more similar for PIs shorter than 50–60 ms (approximately 17–20 sounds/s).

Figure 7. Average Turn Rate

Plots mean turning rate of the flying bats in the three clutter conditions (10 cm, n = 7; 20 cm, n = 23; 40 cm, n = 29 trials included in the analysis) and the open room ( n = 10 trials), referenced to target contact time (zero on the abscissa). There was a significant difference in the bat's turning rate between clutter and open room conditions in the final 100 ms before target contact ( F = 4.78, p < 0.05).

Figure 8. Average Buzz Duration

Plots the mean duration of the buzzes that preceded capture attempts in the open room ( n = 27) and for each of the three target–clutter separations: 10 cm ( n = 2), 20 cm ( n = 23), and 40 cm ( n = 32); n is number of buzzes recorded in trials with good signal-to-noise-ratio sound recordings. Only buzz II (PIs of less than 8 ms [ 10]) was included in this analysis.

Figure 9. Signal Parameters

Summarizes average signal parameters measured in 100-ms time intervals before capture in the open room and for each of the clutter conditions: 10-cm ( n = 7), 20-cm ( n = 25), and 40-cm ( n = 34) target–clutter separations and open room ( n = 11); n is number of trials included in the analyses. Those included had good signal-to-noise ratios, permitting reliable analysis of bat sonar cries throughout the trial. (A) and (B) show temporal parameters (duration and PI), and (C–E) show spectral parameters, start frequency, end frequency, and bandwidth of the fundamental. (F) shows sweep rate. There was a statistically significant main effect of clutter condition on PI ( F = 12.41, p < 0.001) but not on other sound parameters (see text for details on the ANOVA).

Figure 10. Sonar Strobing Behavior

Summarizes the analysis of sonar strobing behavior (see text for definition) in bats attempting insect capture under different clutter conditions. Included in the analyses summarized in (A), (C), and (E) are data from trials in which the bat hit or captured the insect positioned 20 cm from the clutter (17 trials), 40 cm from the clutter (25 trials), and the open room (11 trials). There were too few successful trials at 10 cm to include in these analyses. Note that the time axes differ across plots in this figure. (A) Shows the mean percentage of time the bats produced sonar strobe groups during the 1,000-ms time period before target contact. Data points plot the mean percentage time strobing at midpoints of 200-ms intervals (e.g., data point at −300 ms shows the mean percentage time strobing between the time interval 200–400 ms before target contact). Note that the highest incidence of strobing at 900 ms or more before contact occurred when the bat encountered the target 20 cm from the clutter. (B) Plots the PIs of successive sounds taken from a single trial, showing changes that occur in the temporal patterning of vocalizations before target contact. The strobe groups are circled in red. (C) Plots the mean PIs of sounds contained within strobe groups under open room and clutter conditions, averaged across 100-ms time intervals during the time period 600–200 ms before target contact. For example, the data point at −350 ms shows the mean strobe PI between −300 and −400 ms. (D) Time waveforms of sonar strobe groups taken from the data shown in (B) are displayed. The strobe groups are circled. Measurement of strobe PI is indicated in one of these strobe groups. (E) Plots the mean duration of sounds contained in strobe groups for the clutter and open room conditions, again referenced to target contact time and averaged over 100-ms time bins. (F) Illustrates the measurement of strobe sound duration for one of the sounds in the strobe groups shown above in (D).