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Doppler-shift compensation behavior in horseshoe bats revisited: auditory feedback controls both a decrease and an increase in call frequency
1 Department of Biology, University of California at Riverside, Riverside,
CA 92521-0427, USA
2 Institute of Zoology, Chinese Academy of Sciences, 19 Zhongguancun Road,
Beijing 100080, China
* Present address: Department of Physiological Science, University of California
at Los Angeles, Los Angeles, CA 90095-1606, USA
(e-mail: metzner{at}ucla.edu )
Accepted 20 March 2002
Among mammals, echolocation in bats illustrates the vital role of proper audio-vocal feedback control particularly well. Bats adjust the temporal, spectral and intensity parameters of their echolocation calls depending on the characteristics of the returning echo signal. The mechanism of audio-vocal integration in both mammals and birds is, however, still largely unknown. Here, we present behavioral evidence suggesting a novel audio-vocal control mechanism in echolocating horseshoe bats (Rhinolophus ferrumequinum). These bats compensate for even subtle frequency shifts in the echo caused by flight-induced Doppler effects by adjusting the frequency of their echolocation calls. Under natural conditions, when approaching background targets, the bats usually encounter only positive Doppler shifts. Hence, we commonly believed that, during this Doppler-shift compensation behavior, horseshoe bats use auditory feedback to compensate only for these increases in echo frequency (=positive shifts) by actively lowering their call frequency below the resting frequency (the call frequency emitted when not flying and not experiencing Doppler shifts). Re-investigation of the Doppler-shift compensation behavior, however, shows that decreasing echo frequencies (=negative shifts) are involved as well: auditory feedback from frequencies below the resting frequency, when presented at similar suprathreshold intensity levels as higher echo frequencies, cause the bat's call frequency to increase above the resting frequency. However, compensation for negative shifts is less complete than for positive shifts (22% versus 95%), probably because of biomechanical restrictions in the larynx of bats. Therefore, Doppler-shift compensation behavior involves a quite different neural substrate and audio-vocal control mechanism from those previously assumed. The behavioral results are no longer consistent with solely inhibitory feedback originating from frequencies above the resting frequency. Instead, we propose that auditory feedback follows an antagonistic push/pull principle, with inhibitory feedback lowering and excitatory feedback increasing call frequencies. While the behavioral significance of an active compensation for echo frequencies below RF remains unclear, these behavioral results are crucial for determining the neural implementation of audio-vocal feedback control in horseshoe bats and possibly in mammals in general.
Key words: horseshoe bat, Rhinolophus ferrumequinum, hearing, echolocation, audio-vocal feedback, Doppler-shift compensation behaviour
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