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. The sharp-
basic feature at the root of the evolutionary tree of the ness of delay tuning (50% width) is similar in IC, MGB
sister groups of Phyllostomatidae, to which C. perspicillata and AC [15,26,35,37]. Furthermore, the range of CDs is
belongs, and the Mormoopidae with the genus Pteronotus similar in IC, MGB, and AC with an overrepresentation of
[see 23 ]. This hypothesis is strengthened by the pre- delays from 1 to 10 ms [15,26].
sence of chronotopic cortex organization in other phyl-
lostomids [24 ]. Cortical delay-tuned responses, on the other hand
have certain response features and show interactions
that are not yet present at lower levels and could have
Generation of cortical chronotopy been implemented with the help of a chronotopic
In bat species that have cortical chronotopy, the gener- gradient:
ation of echo delay maps takes place through spatial Among those are a higher specificity regarding stimulus
sorting, and hence transformation of neuronal projections type in P. parnellii for FM stimulus pairs and less
from inferior colliculus (where there is no map, see below) responsiveness to single FM components or to pure
to auditory thalamus and cortex. tone stimuli than in the IC and MGB [14,27 ,37,38].
However, in this respect cortical delay-tuned neurons
The building blocks of cortical chronotopic maps are in C. perspicillata are clearly less specific and they all
delay-sensitive neuronal interactions occurring at subcor- respond vigorously to single pure tones [39 ].
tical levels. For P. parnellii it has been demonstrated that Mechanisms of lateral inhibition and excitatory
facilitatory delay-sensitivity in the ascending auditory feedback that sharpen or shift response tuning are
system first emerges at the level of the central nucleus one of the major advantages of a map, and could be
of the inferior colliculus (ICc; [25,26, review: 27 ]). used to provide dynamic plasticity of receptive fields
Paradoxically, the main components of creation of facil- during learning or arousal [40]. There is ample
itatory delay-sensitivity in ICc are glycinergic inputs evidence from the work of Suga and colleagues on
[28,27 ]. In addition, the ICc inherits a delay-tuned plasticity of neuronal tuning both in tonotopic and in
inhibition from the intermediate nucleus of the lateral target range sensitive cortical areas in P. parnellii.
lemniscus (INLL), conveyed via an excitatory glutami- They showed that a combination of widespread lateral
nergic input [28–32]. Within the ICc, delay tuned neurons inhibition in the cortex and highly focused excitatory
are integrated in the tonotopic representation and are not feedback via projections to other cortical or sub-
arranged according to CD [33], and they also can be tuned cortical areas creates a self-organizing map [8 ,41].
to sound duration [34]. The tectothalamic projection Cortical neurons within this map that code beha-
creates spatially discrete assemblies of delay-tuned viourally important stimuli, can augment the activity
neurons in two regions of the rostral half of the medial of neurons with a similar, ‘matched’ CD in the target
geniculate body (MGB) that are organized according to area and also recruit additional neurons while activity
harmonic frequency bands (FM2, 3, 4). Furthermore, of unmatched neurons is reduced. For the intra-
there is a crude representation of characteristic delay in cortical interaction between the 3 target distance
MGB [35, for further references see 27 ]. maps, this type of ‘egocentric selection’ has been
demonstrated by local cortical electrical activation
Thalamocortical projections feed three discrete ranging [42–45]: The FM-FM area predominantly maintains
areas in AC of P. parnellii. The FM-FM-area and the VF a strong suppressive influence on unmatched
receive overlapping projections from rostral MGB derived neurons in the other two areas and on the
mainly from lateral parts, whereas the DF receives input contralateral FM-FM area. This suppression can
from medial parts [36]. Since there are massive cortico- also result in a shift of the CD of the unmatched
thalamic backprojections, the cortex could also imprint its neurons away from the CD of the FM-FM neuron
chronotopic organization onto its main input structure. So (centrifugal CD shift). In contrast, the DF and VF
far, specific functional roles have not been assigned to the areas have a mostly augmenting influence on
multiple delay representations. matched neurons in the FM-FM area. This can
Figure 3 Legend Target range maps in different bat species. Left: representative spectrograms of echolocation calls. Middle: brain overview with the
position of auditory cortex. Right: detailed view of chronotopic maps within auditory cortex. Target range computing areas are in blue, white arrows
give direction of representation of decreasing echo delay. Black arrows indicate increasing characteristic frequency in tonotopic areas. Please note
that in E. fuscus and M. lucifugus, delay-sensitive neurons are not arranged in a chrontopic map but are interspersed within the tonotopic cortex.
Cortex data are from Schuller et al. [18], Suga [12], Hechavarria et al. [23 ], Hagemann et al. [22 ], Dear et al. [21], Wong and Shannon [19]. Calls for R.
rouxi were kindly provided by D. Leipert, calls for M. lucifugus by B. Fenton, calls from E. fuscus by M. Gadziola.
www.sciencedirect.com Current Opinion in Neurobiology 2014, 24:68–75
72 Neural maps
shift the CD of matched neurons closer to the CD of specific delay but also to the specific temporal syntax of
the DF or VF neuron (centripetal CD shift). The syllables within communication sounds [50,51].
latter could produce a focussing on and sharpening
of tuning to short echo delays in the FM-FM area,
Chronotopic maps as interface to spatial-
since the mapped delay range in DF and VF is
memory, decision-making, and motor-control
restricted to shorter delays in comparison to the FM- systems?
FM area [see 8 ].
Chronotopic maps of target distance that, depending on
This form of self-organizing feedback interaction is a
the echolocation situation, plastically adjust to most
quite powerful general neuronal organization principle
relevant input features (see above) could also provide
and is also found in the interaction between cortex and
an efficient interface to other cortical processing systems.
ICc and MGB [46,47]. In general, the dominance of
Completely unknown is the transfer of spatial infor-
centrifugal plasticity could shape the selective neural
mation from target distance maps to hippocampal place
representation of a specific target distance and produce
cells that in bats have features comparable to those in
contrast enhancement. Dominance of centripetal
rodents [52,53 ].
actions could result in strong clustering and expand
the representation of a selected specific target
A chronotopically organized target distance representa-
distance.
tion could provide an efficient interface to the motor
In P. parnellii, P. quadridens, and C. perspicillata, a
system, in particular since there are target-distance
substantial proportion of cortical delay-tuned
specific behaviours. Most notable is the switch from
neurons, in particular those responding to longer
low call repetition rates during the approach phase of
delays at threshold have a tilted receptive field that
echolocation to high call repetition rates in the final
could allow a certain degree of target tracking
phase shortly before the insect is caught. The wing
(Figure 2, [39 ,23 ]). When the bat approaches its
control breaking behaviour close to obstacles (alarm
target, echo intensity increases due to decreasing
hypothesis, [18]) is also target-distance specific. Both
target-range. As a consequence, during the end stage
types of behaviour should be triggerable by short echo
of approach, only those neurons with appropriately
delays, and the above mentioned intracortical positive
tilted receptive field will continue to respond to
feedback systems that enhance activity to short echo
louder echoes at shorter delays. In this respect tilted
delays may be especially efficient for inducing those
receptive fields loose specificity in terms of static
behaviours. There are also specific reactions to conspe-
object distance but gain specificity in terms of
cifics if they fly close by [54].
responding to echo series that are typical for approach
to target — and may facilitate target tracking. We note
A chronotopic representation may also offer advantages
that some bat species reduce call intensity [48], and
for efficient input from decision-making systems. The
then this sort of tracking at the level of individual
neurons in the FM-FM area that respond both to
neurons would not work. For P. parnellii tilted
call-echo pairs of specific delay and to complex communi-
response areas are present in the FM-FM area but
cation signals may have input from auditory regions of
are not found in the IC [49 ]. They could be generated
frontal cortex [55,56]. It is still to be tested if frontal cortex
within the topographic gradient of the map if there is a
could initiate a switching between both processing modes
level-dependent asymmetry of input convergence or
in the FM-FM area.
input integration in cortical neurons.
Map topography could also provide a more effective
But how are bats without target-distance
means to exert local and delay-specific gain regulation
maps coping?
by modulation through local GABAergic interneurons
In two insectivorous bat species that exclusively use FM
or external modulatory systems.
echolocation signals and that predominantly hunt in open
Additional parameter representation: A 2D repres-
uncluttered space, target distance maps have not been
entation of a single parameter (echo delay) in principle
demonstrated. In E. fuscus (Figure 3) delay-sensitive
allows arranging additional axes orthogonal to the map
neurons are clustered mainly between two tonotopic areas
to represent/process other features. In the FM-FM and
and are interspersed with neurons sensitive to single pure
DF areas of P. parnellii, the three relevant frequency
tones. In M. lucifugus the cortical location of those neurons
bands of the echo harmonics (FM2, 3, 4) are separated
overlaps with tonotopically arranged neurons. The
and projected orthogonal to the delay axis [14,15]. Such
absence of a delay map in E. fuscus has inspired research-
a harmonic dissociation is not found in P. quadridens or
ers to develop an alternative model for cortical repres-
C. perspicillata and in R. rouxi there are no relevant
entation of target distance and acoustic scenes based on
multiple harmonics in the echo.
ensemble coding over a larger number of neurons
Chronotopic maps could also serve non-target relevant
[20 ,57,58 ,59 ]. It also has been demonstrated that
purposes: In P. parnellii, neurons in the FM-FM area
the population of cortical neurons tuned to echo-delay
not only respond well to FM pulse-echo pairs of
could integrate information from objects with different
Current Opinion in Neurobiology 2014, 24:68–75 www.sciencedirect.com
Target range maps in echolocating bats Ko¨ ssl et al. 73
space-depths for the formation of acoustic images. The References and recommended reading
Papers of particular interest, published within the period of review,
latter mechanism can manage a quite powerful processing
have been highlighted as:
of realistic echolocation call/echo sequences [59 ] and it
could also be present in the cortex of bat species that have of special interest
of outstanding interest
a delay map [60]. Therefore, at present there is still an
open discussion if delay maps are strictly necessary for
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