Representation of three-dimensional space in the auditory cortex of the echolocating bat P. discolor

Abstract

The auditory cortex is an essential center for sound localization. In echolocating bats, combination sensitive neurons tuned to specific delays between call emission and echo perception represent target distance. In many bats, these neurons are organized as a chronotopically organized map of echo delay. However, it is still unclear to what extend these neurons can process directional information and thereby form a three-dimensional representation of space. We investigated the representation of three-dimensional space in the auditory cortex of Phyllostomus discolor. Specifically, we hypothesized that combination sensitive neurons encoding target distance in the AC can also process directional information. We used typical echolocation pulses of P. discolor combined with simulated echoes from different positions in virtual 3D-space and measured the evoked neuronal responses in the AC of the anesthetized bats. Our results demonstrate that combination sensitive neurons in the AC responded selectively to specific positions in 3-D space. While these neurons were sharply tuned to echo delay and formed a precise target distance map, the neurons’ specificity in azimuth and elevation depended on the presented sound pressure level. Our data further reveal a topographic distribution of best elevation of the combination sensitive neurons along the rostro-caudal axis i.e., neurons in the rostral part of the target distance map representing short delays prefer elevations below the horizon. Due to their spatial directionality and selectivity to specific echo delays representing target distance, combination sensitive cortical neurons are suited to encode three-dimensional spatial information.

The pale spear‐nosed bat: A neuromolecular and transgenic model for vocal learning

“…Since electrophysiology is routinely employed in bats, we refer to the primary papers rather than presenting such data herein (e.g., Refs. 54 , 55 , 56 , 57 , 58 ). Instead, we focus here on our recent neuroimaging, tracing, and genetic mapping approaches.…”

“…These studies have led to a much greater understanding of the regions of the brain and neural circuitry involved in auditory perception, process-color, including electrophysiology, neuroimaging, connectivity tracing, and histology. Since electrophysiology is routinely employed in bats, we refer to the primary papers rather than presenting such data herein (e.g., Refs [54][55][56][57][58]…”

Cyto- and myeloarchitectural brain atlas of the pale spear-nosed bat (Phyllostomus discolor) in CT Aided Stereotaxic Coordinates

“…This profile-oriented stereotaxic procedure was described in detail in Schuller et al ( 1986 ) and is recommended as standard adjustment procedure. It has been successfully used in Phyllostomus discolor in many studies involving forebrain and midbrain structures (Borina et al 2008 , 2011 ; Bartenstein et al 2014 ; Fenzl and Schuller 2002 , 2005 ; Firzlaff and Schuller 2007 ; Firzlaff et al 2006 , 2007 ; Greiter and Firzlaff 2017a , b ; Genzel et al 2015 ; Heinrich et al 2011 ; Hörpel and Firzlaff 2019 ; Hoffmann et al 2008a , b , 2010 , 2013 , 2015 , 2016 , 2019 ). These studies used a lab-internal series of Nissl stained sections that were relocatable to the present atlas series and fitted to the skull profile used here.…”

“…Phyllostomus discolor is well established as an animal model for behavioral and neurobiological research on echolocation and social communication. The peripheral and central auditory system, the vocal motor system and the visual system of Phyllostomus discolor have been the subject of intense research over the last decades (peripheral and central auditory system: Bartenstein et al 2014 ; Esser and Kiefer 1996 ; Firzlaff et al 2007 ; Firzlaff and Schuller 2003 ; Goerlitz et al 2008 ; Greiter and Firzlaff 2017a , b ; Heinrich et al 2011 ; Hoffmann et al 2008a , b ; Linnenschmidt and Wiegrebe 2019 ; Vanderelst et al 2010 ; vocal motor system: Fenzl and Schuller 2002 ; Fenzl and Schuller 2005 ; visual system: Hoffmann et al 2016 , 2019 ; Kugler et al 2019 ; Rother and Schmidt 1982 ). However, as no brain atlas for Phyllostomus discolor has previously been published, only one of the earlier studies mentioned above involved neuroanatomy beyond basic localization of recording sites.…”

Symmetry and Network Topology in Neuronal Circuits: Complicity of Form and Function

“…[Dear et al, 1993] report structural similarities between bat auditory cortex and mammalian visual cortex. The cover of that issue of Nature made the point more pithily: "How bats' ears see" [Greiter & Firzlaff, 2017] investigate the representation of threedimensional space in the auditory cortex of the bat Phyllostomus discolor. Their observations demonstrate that neurons in the cortex respond to specific positions in space, so they can encode three-dimensional spatial information.…”