Perceptual strategies in active and passive hearing of neotropical bats

Basic spectral and temporal sound properties, such as frequency content and timing, are evaluated by the auditory system to build an internal representation of the external world and to generate auditory guided behaviour. Using echolocating bats as model system, I investigated aspects of spectral and temporal processing during echolocation and in relation to passive listening, and the echo-acoustic object recognition for navigation. In the first project (chapter 2), the spectral processing during passive and active hearing was compared in the echolocting bat Phyllostomus discolor. Sounds are ubiquitously used for many vital behaviours, such as communication, predator and prey detection, or echolocation. The frequency content of a sound is one major component for the correct perception of the transmitted information, but it is distorted while travelling from the sound source to the receiver. In order to correctly determine the frequency content of an acoustic signal, the receiver needs to compensate for these distortions. We first investigated whether P. discolor compensates for distortions of the spectral shape of transmitted sounds during passive listening. Bats were trained to discriminate lowpass filtered from highpass filtered acoustic impulses, while hearing a continuous white noise background with a flat spectral shape. We then assessed their spontaneous classification of acoustic impulses with varying spectral content depending on the background’s spectral shape (flat or lowpass filtered). Lowpass filtered noise background increased the proportion of highpass classifications of the same filtered impulses, compared to white noise background. Like humans, the bats thus compensated for the background’s spectral shape. In an active-acoustic version of the identical experiment, the bats had to classify filtered playbacks of their emitted echolocation calls instead of passively presented impulses. During echolocation, the classification of the filtered echoes was independent of the spectral shape of the passively presented background noise. Likewise, call structure did not change to compensate for the background’s spectral shape. Hence, auditory processing differs between passive and active hearing, with echolocation representing an independent mode with its own rules of auditory spectral analysis. The second project (chapter 3) was concerned with the accurate measurement of the time of occurrence of auditory signals, and as such also distance in echolocation. In addition, the importance of passive listening compared to echolocation turned out to be an unexpected factor in this study. To measure the distance to objects, called ranging, bats measure the time delay between an outgoing call and its returning echo. Ranging accuracy received considerable interest in echolocation research for several reasons: (i) behaviourally, it is of importance for the bat’s ability to locate objects and navigate its surrounding, (ii) physiologically, the neuronal implementation of precise measurements of very short time intervals is a challenge and (iii) the conjectured echo-acoustic receiver of bats is of interest for signal processing. Here, I trained the nectarivorous bat Glossophaga soricina to detect a jittering real target and found a biologically plausible distance accuracy of 4–7 mm, corresponding to a temporal accuracy of 20–40 μs. However, presumably all bats did not learn to use the jittering echo delay as the first and most prominent cue, but relied on passive acoustic listening first, which could only be prevented by the playback of masking noise. This shows that even a non-gleaning bat heavily relies on passive acoustic cues and that the measuring of short time intervals is difficult. This result questions other studies reporting a sub-microsecond time jitter threshold. The third project (chapter 4) linked the perception of echo-acoustic stimuli to the appropriate behavioural reactions, namely evasive flight manoeuvres around virtual objects presented in the flight paths of wild, untrained bats. Echolocating bats are able to orient in complete darkness only by analysing the echoes of their emitted calls. They detect, recognize and classify objects based on the spectro-temporal reflection pattern received at the two ears. Auditory object analysis, however, is inevitably more complicated than visual object analysis, because the one-dimensional acoustic time signal only transmits range information, i.e., the object’s distance and its longitudinal extent. All other object dimensions like width and height have to be inferred from comparative analysis of the signals at both ears and over time. The purpose of this study was to measure perceived object dimensions in wild, experimentally naive bats by video-recording and analysing the bats’ evasive flight manoeuvres in response to the presentation of virtual echo-acoustic objects with independently manipulated acoustic parameters. Flight manoeuvres were analysed by extracting the flight paths of all passing bats. As a control to our method, we also recorded the flight paths of bats in response to a real object. Bats avoided the real object by flying around it. However, we did not find any flight path changes in response to the presentation of several virtual objects. We assume that the missing spatial extent of virtual echo-acoustic objects, due to playback from only one loudspeaker, was the main reason for the failure to evoke evasive flight manoeuvres. This study therefore emphasises for the first time the importance of the spatial dimension of virtual objects, which were up to now neglected in virtual object presentations.