Echo-acoustic flow shapes object representation in spatially complex acoustic scenes

Abstract

Echolocating bats use echoes of their sonar emissions to determine the position and distance of objects or prey. Target distance is represented as a map of echo delay in the auditory cortex (AC) of bats. During a bat's flight through a natural complex environment, echo streams are reflected from multiple objects along its flight path. Separating such complex streams of echoes or other sounds is a challenge for the auditory system of bats as well as other animals. We investigated the representation of multiple echo streams in the AC of anesthetized bats () and tested the hypothesis that neurons can lock on echoes from specific objects in a complex echo-acoustic pattern while the representation of surrounding objects is suppressed. We combined naturalistic pulse/echo sequences simulating a bat's flight through a virtual acoustic space with extracellular recordings. Neurons could selectively lock on echoes from one object in complex echo streams originating from two different objects along a virtual flight path. The objects were processed sequentially in the order in which they were approached. Object selection depended on sequential changes of echo delay and amplitude, but not on absolute values. Furthermore, the detailed representation of the object echo delays in the cortical target range map was not fixed but could be dynamically adapted depending on the temporal pattern of sonar emission during target approach within a simulated flight sequence. Complex signal analysis is a challenging task in sensory processing for all animals, particularly for bats because they use echolocation for navigation in darkness. Recent studies proposed that the bat's perceptional system might organize complex echo-acoustic information into auditory streams, allowing it to track specific auditory objects during flight. We show that in the auditory cortex of bats, neurons can selectively respond to echo streams from specific objects.

Echo-acoustic and optic flow interact in bats

“…For example, distance information is readily available to bats by analysing the delay between call emission and arrival of the reflected echoes. The bats' central nervous system has evolved special adaptations for the processing of echo-delay information, resulting in a chronotopic map in the auditory cortex (Greiter and Firzlaff, 2017;Hagemann et al, 2010;Suga and O'Neill, 1979). However, our results demonstrate behavioural correlates of audiovisual integration that are comparable to results from 'classical' studies on multimodal integration in animals with less-specialized sensory systems.…”

Mapping the distribution of language related genes FoxP1, FoxP2, and CntnaP2 in the brains of vocal learning bat species

“…In P. discolor juveniles however, cortical staining was strongly enriched in deep layers of the primary auditory cortex and posterior dorsal field (PDF) of the auditory cortex, suggesting that FoxP2 could play a role in postnatal development of these brain regions. Of note, the PDF of the P. discolor auditory cortex contains combination sensitive neurons that form a chronotopic map of echo delay (Greiter & Firzlaff, 2017). In the mustached bat (Pteronotus parnellii), neurons in comparable regions of the auditory cortex are specialized for processing communication calls (Ohlemiller, Kanwal, & Suga, 1996) and are sensitive to the combinations of, and temporal relationships between, syllables of these calls (Ohlemiller et al, 1996;Esser, Condon, Suga, & Kanwal, 1997).…”

Processing of temporally patterned sounds in the auditory cortex of Seba's short‐tailed bat,Carollia perspicillata

“…The aim of the present study was to characterize temporal information processing in AC neurons of bats, a highly vocal animal group. For over 50 years, bats have been used as an animal model to study the auditory system and its function (Feng et al, 1978;Zhang et al, 1997;Covey & Casseday, 1999;Suga & Ma, 2003;K€ ossl et al, 2012;Wohlgemuth et al, 2016;Greiter & Firzlaff, 2017). Bat auditory neurons are able to encode temporal cues such as the timing from call emission to echo arrival (so-called echo delay), which aids the bat in target distance estimation, that is, the longer the echo delay, the farther away the target (Suga & O'Neill, 1979;Yan & Suga, 1996;Portfors & Wenstrup, 1999;Hagemann et al, 2011;Hechavarr ıa et al, 2013).…”