Edited by James A. Simmons, Brown University, Providence, RI, and accepted by Editorial Board Member Thomas D. Albright April 30, 2019 (received for review January 26, 2019)
Many animal species are known for unparalleled abilities to encode sensory information that supports fast, reliable action in complex environments, but the mechanisms remain often unclear. Here, we present a nonlinear principle for sensory information encoding in bats. Through fast ear motions, bats can encode information on target direction into time-frequency Doppler signatures. These species were thought to be evolutionarily tuned to Doppler shifts generated by a prey’s wing beat. Self-generated Doppler shifts from the bat’s own flight motion were, for the most part, considered a nuisance that the bats compensate for. Our findings indicate that these Doppler-based biosonar systems may be more complicated than previously thought because the animals can actively inject Doppler shifts into their input signals.
Many animals have evolved adept sensory systems that enable dexterous mobility in complex environments. Echolocating bats hunting in dense vegetation represent an extreme case of this, where all necessary information about the environment must pass through a parsimonious channel of pulsed, 1D echo signals. We have investigated whether certain bats (rhinolophids and hipposiderids) actively create Doppler shifts with their pinnae to encode additional sensory information. Our results show that the bats’ active pinna motions are a source of Doppler shifts that have all attributes required for a functional relevance: (i) the Doppler shifts produced were several times larger than the reported perception threshold; (ii) the motions of the fastest moving pinna portions were oriented to maximize the Doppler shifts for echoes returning from the emission direction, indicating a possible evolutionary optimization; (iii) pinna motions coincided with echo reception; (iv) Doppler-shifted signals from the fast-moving pinna portion entered the ear canal of a biomimetic pinna model; and (v) the time-frequency Doppler shift signatures were found to encode target direction in an orderly fashion. These results indicate that instead of avoiding or suppressing all self-produced Doppler shifts, rhinolophid and hipposiderid bats actively create Doppler shifts with their own pinnae. These bats could hence make use of a previously unknown nonlinear mechanism for the encoding of sensory information, based on Doppler signatures. Such a mechanism could be a source for the discovery of sensing principles not only in sensory physiology but also in the engineering of sensory systems.
↵1X.Y. and R.M. contributed equally to this work.
Author contributions: X.Y. and R.M. designed research; X.Y. performed research; X.Y. and R.M. analyzed data; and X.Y. and R.M. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission. J.A.S. is a Guest Editor invited by the Editorial Board.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1901120116/-/DCSupplemental.
Published under the PNAS license.
