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Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved February 20, 2015 (received for review December 21, 2014)
Significance
Echolocating bats and toothed whales emit a terminal buzz right before capture. The high call rate (≥180 Hz) and short duration should preclude informed reactions, leaving the ubiquitous buzz an enigma. By removing prey from bats right before capture, we showed that the buzz is not inflexible but adaptable and that bats react on a very fast time scale to sudden changes in perceptual feedback. Acoustic and behavioral reactions differed, indicating separate central control of echolocation and capture movements, as well as importance of somatosensory feedback. These results in a naturally behaving animal relying on multimodal integration of actively controlled senses are significant for a central problem in neurobiology: fast decision making.
Abstract
Echolocation is an active sense enabling bats and toothed whales to orient in darkness through echo returns from their ultrasonic signals. Immediately before prey capture, both bats and whales emit a buzz with such high emission rates (≥180 Hz) and overall duration so short that its functional significance remains an enigma. To investigate sensory–motor control during the buzz of the insectivorous bat Myotis daubentonii, we removed prey, suspended in air or on water, before expected capture. The bats responded by shortening their echolocation buzz gradually; the earlier prey was removed down to approximately 100 ms (30 cm) before expected capture, after which the full buzz sequence was emitted both in air and over water. Bats trawling over water also performed the full capture behavior, but in-air capture motions were aborted, even at very late prey removals (<20 ms = 6 cm before expected contact). Thus, neither the buzz nor capture movements are stereotypical, but dynamically adapted based on sensory feedback. The results indicate that echolocation is controlled mainly by acoustic feedback, whereas capture movements are adjusted according to both acoustic and somatosensory feedback, suggesting separate (but coordinated) central motor control of the two behaviors based on multimodal input. Bat echolocation, especially the terminal buzz, provides a unique window to extremely fast decision processes in response to sensory feedback and modulation through attention in a naturally behaving animal.
Footnotes
↵1C.G., S.B., L.W., and A.S. contributed equally to this work.
- ↵2To whom correspondence should be addressed. Email: ams{at}biology.sdu.dk.
Author contributions: C.G., S.B., L.W., and A.S. designed research; performed research; analyzed data; and wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1424457112/-/DCSupplemental.
Function of terminal buzz in echolocating bats
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