Neural Processing of Naturalistic Echolocation Signals in Bats

Abstract

Echolocation behavior, a navigation strategy based on acoustic signals, allows scientists to explore neural processing of behaviorally relevant stimuli. For the purpose of orientation, bats broadcast echolocation calls and extract spatial information from the echoes. Because bats control call emission and thus the availability of spatial information, the behavioral relevance of these signals is undiscussable. While most neurophysiological studies, conducted in the past, used synthesized acoustic stimuli that mimic portions of the echolocation signals, recent progress has been made to understand how naturalistic echolocation signals are encoded in the bat brain. Here, we review how does stimulus history affect neural processing, how spatial information from multiple objects and how echolocation signals embedded in a naturalistic, noisy environment are processed in the bat brain. We end our review by discussing the huge potential that state-of-the-art recording techniques provide to gain a more complete picture on the neuroethology of echolocation behavior.

The influence of stimulus history on directional coding in the monarch butterfly brain

“…1 , 2 ). A similar effect on tuning sharpness has been reported in the mammalian cortex when the animals were stimulated with sequenced stimuli rather than with an isolated stimulus (Wehr and Zador 2005 ; Beetz and Hechavarría 2022 ). For example, the spatial tuning of auditory neurons is sharper when bats are stimulated with sequences of echolocation signals rather than temporally isolated acoustic signals (Beetz et al 2016a , 2017 ).…”

“…However, in nature, cues are usually not processed as discrete events in time but rather form a continuous perception of the cue. Therefore, it is not surprising that many neurons are highly sensitive to the stimulus history and integrate information from subsequent stimuli (Clark and Demb 2016 ; Weber et al 2019 ; Jin and Glickfeld 2020 ; Benda 2021 ; López-Jury et al 2021 ; Beetz and Hechavarría 2022 ; Pastyrik and Firzlaff 2022 ; Price and Gavornik 2022 ). Here, we explicitly tested how the stimulus history, i.e., angular velocity and trajectory of a compass cue, affects the directional coding in the monarch butterfly brain.…”

A perspective on neuroethology: what the past teaches us about the future of neuroethology

“…As a PhD student, I shifted my focus from invertebrates to vertebrates and conducted neural recordings in echolocating bats. For short-range orientation, bats extract spatial information from echoes (Beetz and Hechavarría 2022). Given that the behavioral relevance of the echolocation signals is clear, I tested how such signals are processed in the bat brain (Beetz et al 2016a, b;.…”

“…Hence, acoustic communication in diverse species is central to the research of many neuroethologists (Kelley 2004;Elie and Theunissen 2020;Römer 2021;Narins et al 2023). However, the acoustic sense is also useful for nocturnal orientation, whether it is used in the context of echolocation in bats (Beetz and Hechavarría 2022) or localizing potential prey by passively listening to prey-emitted sounds (Singheiser et al 2012;Brewton et al 2018). During foraging, chemosensation is also essential to localizing food and determining its quality.…”

“…Bat research represents a good example of how neuroethological topics change over the years. Traditionally, bats were investigated to understand how they negotiate obstacles in darkness without using their eyes (Simmons et al 1978;Neuweiler 2003;Beetz and Hechavarría 2022). This remarkable feat, which is based on a highly specialized auditory sense, has fascinated scientists for decades.…”