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Neural Maps for Target Range in the Auditory Cortex of Echolocating Bats

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Neural Maps for Target Range in the Auditory Cortex of Echolocating Bats Available online at www.sciencedirect.com ScienceDirect Neural maps for target range in the auditory cortex of echolocating bats 1 1 1 2 2 3 M Ko¨ ssl , JC Hechavarria , C Voss , S Macias , EC Mora and M Vater Computational brain maps as opposed to maps of receptor require less genetic information than other wiring surfaces strongly reflect functional neuronal design principles. arrangements [2]. In addition, on a functional level, In echolocating bats, computational maps are established that spatially restricted local neuronal interactions like lateral topographically represent the distance of objects. These target inhibition can be implemented easily within a spatial range maps are derived from the temporal delay between parameter gradient as provided by a map [3,4]. Within emitted call and returning echo and constitute a regular a map, topological substructures like clusters or pin- representation of time (chronotopy). Basic features of these wheels can be created to optimize local function [5]. maps are innate, and in different bat species the map size and As pointed out by Schreiner and Winer [6], map topo- precision varies. An inherent advantage of target range maps is graphies and their connectional metric can also provide a the implementation of mechanisms for lateral inhibition and stable basis for efficient functional transformations and excitatory feedback. Both can help to focus target ranging dynamic remodelling during development, like changing depending on the actual echolocation situation. However, head related transfer functions during head growth or these maps are not absolutely necessary for bat echolocation neuromodulatory control of cortical plasticity [7,8 ]. since there are bat species without cortical target-distance maps, which use alternative ensemble computation Unlike the visual or somatosensory system where import- mechanisms. ant spatial relationships are already mapped on the re- Addresses ceptor surface, spatial auditory information has to be 1 Institute for Cell Biology and Neuroscience, Goethe University, calculated de novo by comparing response properties of Frankfurt, Max-von-Laue-Str. 13, 60439 Frankfurt, Germany 2 both ears and in some species is then represented in Department of Animal and Human Biology, Faculty of Biology, Havana midbrain auditory space maps [1]. In the forebrain such University, calle 25 No. 455 entre J e I, Vedado, CP 10400, Ciudad de La type of continuous spatial map is no longer prominent and Habana, Cuba 3 Institute for Biochemistry and Biology, University of Potsdam, Karl clustered types of representation prevail [e.g. 9]. This is Liebknecht Str. 26, 14476 Golm, Germany also true for bat auditory cortex where clustered binaural interactions [10] and a clustered representation of Corresponding author: Ko¨ ssl, M ([email protected]) dynamic spatial receptive fields could be demonstrated [11]. In the cortex of bats, there are computational maps Current Opinion in Neurobiology 2014, 24:68–75 that contain target-relevant information extracted from returning echoes [review: 12]. There are two major types This review comes from a themed issue on Neural maps of such maps: first, the delay (D) between emitted bio- Edited by David Fitzpatrick and Nachum Ulanovsky sonar signal and returning echo is mapped to derive target For a complete overview see the Issue and the Editorial range (R) with R = D*C/2 (C = sound velocity) (Figure 1). Available online 17th September 2013 Within such a map individual neurons are most sensitive 0959-4388/$ – see front matter, # 2013 Elsevier Ltd. All rights to a specific echo delay that is defined as the characteristic reserved. delay (CD). In the mustached bat, Pteronotus parnellii, a http://dx.doi.org/10.1016/j.conb.2013.08.016 widely used bat model for auditory processing, three target distance maps have been demonstrated in the FM-FM, dorsal fringe and ventral fringe (DF, VF) cor- Introduction tical areas, respectively [13 ,14–16], second, relative velocity between bat and object is mapped in form of Sensory brain maps consist of topographically continuous Doppler-induced echo frequency shifts [17]. In contrast neuronal representations of a certain stimulus feature. to any other receptor-surface-dominated or compu- Such a representation can already be generated at the tational map, input into these maps is actively controlled sensory surface and either reflects spatially continuous by the animal through its echolocation signal emission. sensory input or properties of sensory filtering along the receptor surface like the cochlear hair cells. The other type of map is computational in the sense that it is created Chronotopic target range maps in different in the brain by extracting behaviourally relevant stimulus bat species information [1]. For both types of maps, wiring optimiz- Target range maps were initially discovered by Suga, ation and economy regarding projections between O’Neill and colleagues in the auditory cortex of the mapped areas are an inherent advantage. In this sense, mustached bat P. parnellii by using passive auditory a topographically ordered wiring of brain areas should also stimulation with pairs of frequency modulated (FM) Current Opinion in Neurobiology 2014, 24:68–75 www.sciencedirect.com Target range maps in echolocating bats Ko¨ ssl et al. 69 Figure 1 world long-CF–FM bat where the FM component which is important for target range estimation is preceded by a R = D*C/2 constant frequency (CF) component that is used by the R = target range bat to exploit echo Doppler-shifts to derive information D = echo delay on relative velocity. Velocity sensitive neurons are also C = sound velocity arranged in form of a computational map (P. parnellii: CF– CF area, see Figure 3; [17]). Remarkably, chronotopy has evolved convergently both in old and new world bat families. Rhinolophus rouxi, a bat species from the family call Rhinolophidae that is widely distributed in the old world possesses a target range map located in the dorsal auditory cortex ([18], Figure 3). However, in the auditory cortex of bats, that only employ FM biosonar signals, delay sensi- echo tive neurons are not necessarily arranged in form of target distance maps [19,20 ,21]. In Eptesicus fuscus they form clusters that are located mainly within a high frequency Current Opinion in Neurobiology cortex region where cortical tonotopy reverses ([21]; Figure 3). Only recently were target maps discovered Echolocating bat that computes target range (R) from the echo delay (D). for a frugivorous FM bat, Carollia perspicillata [22 ] and for the insectivorous short-CF–FM bat Pteronotus quad- ridens [23 ]. Interestingly, in C. perspicillata, delay-sensi- sweeps that mimic the FM components of echolocation tive neurons occur in dorsal high frequency areas and signal and echo. Neurons that preferentially respond to a within a region where tonotopy reverses in primary audi- specific echo delay (Figure 2: examples of delay tuning tory cortex, as in E. fuscus (Figure 3). curves from different bat species) are arranged in approxi- mately rostrocaudal direction such that neurons respond- It is still open if the presence of a short or long CF ing to short echo delay and hence short target distances component in the echolocation signal and the accompa- are represented more rostrally than neurons responding to nying added cortical computational complexity long echo delays (Figure 3). The mustached bat is a new encourages the formation of a mapped target range pro- Figure 2 (a) (c) (e) P. parnellii P. quadridens C. perspicillata 90 90 70 70 70 50 50 50 30 30 0 5101520 0 510152025 0 5101520 (b) (d) (f) 90 90 70 70 Echo-level [dB SPL] 70 50 50 50 30 30 30 0 5101520 0 5 10 15 20 25 0 5 10 15 20 echo-delay [ms] Current Opinion in Neurobiology Examples of receptive fields of delay-sensitive neurons in 3 bat species: P. parnellii, P. quadridens, and C. perspicillata. The stimulus consists of a pair of FM sweeps separated by a specific delay that represents sonar pulse and echo. The call level is held constant at 70 or 80 dB SPL, the echo level and delay are varied. Normalized neuronal response strength is color coded, red indicates maximal number of action potentials, the black line indicates 50% of maximal activity. The response area can be echo level invariant (a,c,e) or tilted (b,d,f). Tilt can provide for a certain amount of tracking of approaching objects on a single neuron basis (see text). www.sciencedirect.com Current Opinion in Neurobiology 2014, 24:68–75 70 Neural maps Figure 3 Rhinolophus rouxi FM-FM 100 AI CF/CF 50 D R C frequency [kHz] 0 FA 25 ms V DF Pteronotus parnellii 100 FM-FM CF/CF 50 Ala Alp DSCF frequency [kHz] 0 20 ms VF Pteronotus quadridens 100 FM-FM 50 frequency [kHz] 0 2 ms Carollia perspicillata FM-FM 100 HFII AAF HFI 50 DP AlI frequency [kHz] Al 0 2 ms Myotis lucifugus 100 RA 50 frequency [kHz] 0 2 ms Eptesicus fuscus AI primary auditory cortex AII secondary auditory cortex AAF anterior auditory field 100 CF/CF CF/CF area FM-FM FM-FM area FA fovea area DF dorsal fringe 50 DP dorsoposterior field DSCF doppler-shifted constant frequency field frequency [kHz] 0 HF highfrequency field 2 ms 1 mm 1 mm RA rostral area VF ventral fringe Current Opinion in Neurobiology Current Opinion in Neurobiology 2014, 24:68–75 www.sciencedirect.com Target range maps in echolocating bats Ko¨ ssl et al. 71 cessing area. However, the FM bat C. perspicillata has Emergent features within target distance implemented a prominent target range map in the cortex. maps There are no CF components in the call of C. perspicillata Neural processing to create delay tuning in P. parnellii (Figure 3). This could suggest that chronotopy is a very appears largely complete at subcortical levels.
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