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Research Article

Echolocating bats detect but misperceive a multidimensional incongruent acoustic stimulus

View ORCID ProfileSasha Danilovich, Gal Shalev, View ORCID ProfileArjan Boonman, View ORCID ProfileAya Goldshtein, and View ORCID ProfileYossi Yovel
PNAS November 10, 2020 117 (45) 28475-28484; first published October 26, 2020; https://doi.org/10.1073/pnas.2005009117
Sasha Danilovich
aSagol School of Neuroscience, Tel Aviv University, 6997801 Tel Aviv, Israel;
bDepartment of Zoology, Faculty of Life Sciences, Tel Aviv University, 6997801 Tel Aviv, Israel
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Gal Shalev
bDepartment of Zoology, Faculty of Life Sciences, Tel Aviv University, 6997801 Tel Aviv, Israel
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Arjan Boonman
bDepartment of Zoology, Faculty of Life Sciences, Tel Aviv University, 6997801 Tel Aviv, Israel
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Aya Goldshtein
bDepartment of Zoology, Faculty of Life Sciences, Tel Aviv University, 6997801 Tel Aviv, Israel
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Yossi Yovel
aSagol School of Neuroscience, Tel Aviv University, 6997801 Tel Aviv, Israel;
bDepartment of Zoology, Faculty of Life Sciences, Tel Aviv University, 6997801 Tel Aviv, Israel
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  • ORCID record for Yossi Yovel
  • For correspondence: yossiyovel@gmail.com
  1. Edited by Thomas D. Albright, The Salk Institute for Biological Studies, La Jolla, CA, and approved September 25, 2020 (received for review April 11, 2020)

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Significance

How do we build a perception from incoming sensory information? To accurately perceive the environment, the brain has to integrate information across different sensory modalities and to analyze multiple sensory dimensions within a sensory modality. We studied this integration in echolocating bats, the masters of active acoustic sensing. By presenting them with targets whose acoustic dimensions were incoherent, we managed to induce misperception, which caused the bats to repeatedly try to fly through a wall even though they detected it with their echolocation. We demonstrate that certain relations between the dimensions must hold to allow accurate perception. Nevertheless, adult bats can learn new relations rapidly. Notably, no misperception was observed in pups, confirming that these relations are not innate.

Abstract

Coherent perception relies on integrating multiple dimensions of a sensory modality, for example, color and shape in vision. We reveal how different acoustic dimensions, specifically echo intensity and sonar aperture (or width), are important for correct perception by echolocating bats. We flew bats down a corridor blocked by objects with different intensity–aperture combinations. To our surprise, bats crashed straight into large (aperture) walls with weak echo intensity as if they did not exist. The echolocation behavior of the bats indicated that they did detect the wall, suggesting that crashing was not a result of limited sensory sensitivity, but of a perceptual deficit. We systematically manipulated intensity and aperture by changing the materials and width of different reflectors, and we conclude that a coherent echo-based percept is created only when these two acoustic dimensions have certain relations which are typical for objects in nature (e.g., large and intense or small and weak reflectors). Nevertheless, we show that these preferred relations are not innate. We show that young pups are not constrained to these relations and that new intensity–aperture associations can also be learned by adult bats.

  • perception
  • sensory integration
  • bats
  • echolocation

Footnotes

  • ↵1To whom correspondence may be addressed. Email: yossiyovel{at}gmail.com.
  • Author contributions: S.D. and Y.Y. designed research; S.D., G.S., A.B., A.G., and Y.Y. performed research; S.D. analyzed data; and S.D. and Y.Y. wrote the paper.

  • The authors declare no competing interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.2005009117/-/DCSupplemental.

Data Availability.

The data, methods, and code are available in the main text and SI Appendix.

Published under the PNAS license.

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Echolocating bats detect but misperceive a multidimensional incongruent acoustic stimulus
Sasha Danilovich, Gal Shalev, Arjan Boonman, Aya Goldshtein, Yossi Yovel
Proceedings of the National Academy of Sciences Nov 2020, 117 (45) 28475-28484; DOI: 10.1073/pnas.2005009117

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Echolocating bats detect but misperceive a multidimensional incongruent acoustic stimulus
Sasha Danilovich, Gal Shalev, Arjan Boonman, Aya Goldshtein, Yossi Yovel
Proceedings of the National Academy of Sciences Nov 2020, 117 (45) 28475-28484; DOI: 10.1073/pnas.2005009117
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