-
Neural maps for target range in the auditory cortex
ofecholocating batsM Kössl1, JC Hechavarria1, C Voss1, S Macias2,
EC Mora2 and M Vater3
Available online at www.sciencedirect.com
ScienceDirect
Computational brain maps as opposed to maps of receptor
surfaces strongly reflect functional neuronal design
principles.
In echolocating bats, computational maps are established
that
topographically represent the distance of objects. These
target
range maps are derived from the temporal delay between
emitted call and returning echo and constitute a regular
representation of time (chronotopy). Basic features of these
maps are innate, and in different bat species the map size
and
precision varies. An inherent advantage of target range maps
is
the implementation of mechanisms for lateral inhibition and
excitatory feedback. Both can help to focus target ranging
depending on the actual echolocation situation. However,
these maps are not absolutely necessary for bat echolocation
since there are bat species without cortical target-distance
maps, which use alternative ensemble computation
mechanisms.
Addresses1 Institute for Cell Biology and Neuroscience, Goethe
University,
Frankfurt, Max-von-Laue-Str. 13, 60439 Frankfurt, Germany2
Department of Animal and Human Biology, Faculty of Biology,
Havana
University, calle 25 No. 455 entre J e I, Vedado, CP 10400,
Ciudad de La
Habana, Cuba3 Institute for Biochemistry and Biology, University
of Potsdam, Karl
Liebknecht Str. 26, 14476 Golm, Germany
Corresponding author: Kössl, M
([email protected])
Current Opinion in Neurobiology 2014, 24:68–75
This review comes from a themed issue on Neural maps
Edited by David Fitzpatrick and Nachum Ulanovsky
For a complete overview see the Issue and the Editorial
Available online 17th September 2013
0959-4388/$ – see front matter, # 2013 Elsevier Ltd. All
rightsreserved.
http://dx.doi.org/10.1016/j.conb.2013.08.016
IntroductionSensory brain maps consist of topographically
continuousneuronal representations of a certain stimulus
feature.Such a representation can already be generated at
thesensory surface and either reflects spatially continuoussensory
input or properties of sensory filtering along thereceptor surface
like the cochlear hair cells. The othertype of map is computational
in the sense that it is createdin the brain by extracting
behaviourally relevant stimulusinformation [1]. For both types of
maps, wiring optimiz-ation and economy regarding projections
betweenmapped areas are an inherent advantage. In this sense,a
topographically ordered wiring of brain areas should also
Current Opinion in Neurobiology 2014, 24:68–75
require less genetic information than other wiringarrangements
[2]. In addition, on a functional level,spatially restricted local
neuronal interactions like lateralinhibition can be implemented
easily within a spatialparameter gradient as provided by a map
[3,4]. Withina map, topological substructures like clusters or
pin-wheels can be created to optimize local function [5].As pointed
out by Schreiner and Winer [6], map topo-graphies and their
connectional metric can also provide astable basis for efficient
functional transformations anddynamic remodelling during
development, like changinghead related transfer functions during
head growth orneuromodulatory control of cortical plasticity
[7,8��].
Unlike the visual or somatosensory system where import-ant
spatial relationships are already mapped on the re-ceptor surface,
spatial auditory information has to becalculated de novo by
comparing response properties ofboth ears and in some species is
then represented inmidbrain auditory space maps [1]. In the
forebrain suchtype of continuous spatial map is no longer prominent
andclustered types of representation prevail [e.g. 9]. This isalso
true for bat auditory cortex where clustered binauralinteractions
[10] and a clustered representation ofdynamic spatial receptive
fields could be demonstrated[11]. In the cortex of bats, there are
computational mapsthat contain target-relevant information
extracted fromreturning echoes [review: 12]. There are two major
typesof such maps: first, the delay (D) between emitted bio-sonar
signal and returning echo is mapped to derive targetrange (R) with
R = D*C/2 (C = sound velocity) (Figure 1).Within such a map
individual neurons are most sensitiveto a specific echo delay that
is defined as the characteristicdelay (CD). In the mustached bat,
Pteronotus parnellii, awidely used bat model for auditory
processing, threetarget distance maps have been demonstrated in
theFM-FM, dorsal fringe and ventral fringe (DF, VF) cor-tical
areas, respectively [13��,14–16], second, relativevelocity between
bat and object is mapped in form ofDoppler-induced echo frequency
shifts [17]. In contrastto any other receptor-surface-dominated or
compu-tational map, input into these maps is actively controlledby
the animal through its echolocation signal emission.
Chronotopic target range maps in differentbat speciesTarget
range maps were initially discovered by Suga,O’Neill and colleagues
in the auditory cortex of themustached bat P. parnellii by using
passive auditorystimulation with pairs of frequency modulated
(FM)
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Target range maps in echolocating bats Kössl et al. 69
Figure 1
R = D*C/2
R = target rangeD = echo delayC = sound velocity
call
echo
Current Opinion in Neurobiology
Echolocating bat that computes target range (R) from the echo
delay (D).
sweeps that mimic the FM components of echolocationsignal and
echo. Neurons that preferentially respond to aspecific echo delay
(Figure 2: examples of delay tuningcurves from different bat
species) are arranged in approxi-mately rostrocaudal direction such
that neurons respond-ing to short echo delay and hence short target
distancesare represented more rostrally than neurons responding
tolong echo delays (Figure 3). The mustached bat is a new
Figure 2
P. parnellii
echo-d
Ech
o-le
vel [
dB S
PL]
90
70
50
90
70
50
30
90
70
50
30
90
70
50
30
(a) (c)
(b) (d)0 5 10 15 20
0 5 10 15 20 0 5 10
0 5 10
P. qu
Examples of receptive fields of delay-sensitive neurons in 3 bat
species: P. pa
of FM sweeps separated by a specific delay that represents sonar
pulse and e
delay are varied. Normalized neuronal response strength is color
coded, red
50% of maximal activity. The response area can be echo level
invariant (a,c
approaching objects on a single neuron basis (see text).
www.sciencedirect.com
world long-CF–FM bat where the FM component whichis important
for target range estimation is preceded by aconstant frequency (CF)
component that is used by thebat to exploit echo Doppler-shifts to
derive informationon relative velocity. Velocity sensitive neurons
are alsoarranged in form of a computational map (P. parnellii:
CF–CF area, see Figure 3; [17]). Remarkably, chronotopy hasevolved
convergently both in old and new world batfamilies. Rhinolophus
rouxi, a bat species from the familyRhinolophidae that is widely
distributed in the old worldpossesses a target range map located in
the dorsal auditorycortex ([18], Figure 3). However, in the
auditory cortex ofbats, that only employ FM biosonar signals, delay
sensi-tive neurons are not necessarily arranged in form of
targetdistance maps [19,20��,21]. In Eptesicus fuscus they
formclusters that are located mainly within a high frequencycortex
region where cortical tonotopy reverses ([21];Figure 3). Only
recently were target maps discoveredfor a frugivorous FM bat,
Carollia perspicillata [22��] andfor the insectivorous short-CF–FM
bat Pteronotus quad-ridens [23�]. Interestingly, in C.
perspicillata, delay-sensi-tive neurons occur in dorsal high
frequency areas andwithin a region where tonotopy reverses in
primary audi-tory cortex, as in E. fuscus (Figure 3).
It is still open if the presence of a short or long CFcomponent
in the echolocation signal and the accompa-nying added cortical
computational complexityencourages the formation of a mapped target
range pro-
elay [ms]
70
50
30
70
50
30
(e)
(f)
15 20 25
15 20 0 5 10 15 20
0 5 10 15 20
25
adridens C. perspicillata
Current Opinion in Neurobiology
rnellii, P. quadridens, and C. perspicillata. The stimulus
consists of a pair
cho. The call level is held constant at 70 or 80 dB SPL, the
echo level and
indicates maximal number of action potentials, the black line
indicates
,e) or tilted (b,d,f). Tilt can provide for a certain amount of
tracking of
Current Opinion in Neurobiology 2014, 24:68–75
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70 Neural maps
Figure 3
Rhinolophus rouxi FM-FM
FM-FM
FM-FM
FM-FM
CF/CF
FA
CF/CF
Ala
VF
HFII
HFI
DP
Al
AAF
RA
AI
AII
AAF
CF/CF
FM-FM
FADF
DP
DSCF
HF
RA
VF
primary auditory cortex
secondary auditory cortex
anterior auditory field
CF/CF areaFM-FM area
fovea area
dorsal fringe
dorsoposterior field
highfrequency field
rostral area
ventral fringe
doppler-shifted constantfrequency field
AlI
DSCFAlp
DF
D
R C
V
AI
Pteronotus parnellii
Pteronotus quadridens
Carollia perspicillata
Myotis lucifugus
Eptesicus fuscus
100fr
eque
ncy
[kH
z]fr
eque
ncy
[kH
z]fr
eque
ncy
[kH
z]fr
eque
ncy
[kH
z]fr
eque
ncy
[kH
z]fr
eque
ncy
[kH
z]
50
25 ms
20 ms
2 ms
2 ms
0
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50
0
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0
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0
2 ms
2 ms 1 mm 1 mm
100
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0
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0
Current Opinion in Neurobiology
Current Opinion in Neurobiology 2014, 24:68–75
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Target range maps in echolocating bats Kössl et al. 71
cessing area. However, the FM bat C. perspicillata
hasimplemented a prominent target range map in the cortex.There are
no CF components in the call of C. perspicillata(Figure 3). This
could suggest that chronotopy is a verybasic feature at the root of
the evolutionary tree of thesister groups of Phyllostomatidae, to
which C. perspicillatabelongs, and the Mormoopidae with the genus
Pteronotus[see 23�]. This hypothesis is strengthened by the
pre-sence of chronotopic cortex organization in other
phyl-lostomids [24�].
Generation of cortical chronotopyIn bat species that have
cortical chronotopy, the gener-ation of echo delay maps takes place
through spatialsorting, and hence transformation of neuronal
projectionsfrom inferior colliculus (where there is no map, see
below)to auditory thalamus and cortex.
The building blocks of cortical chronotopic maps
aredelay-sensitive neuronal interactions occurring at subcor-tical
levels. For P. parnellii it has been demonstrated thatfacilitatory
delay-sensitivity in the ascending auditorysystem first emerges at
the level of the central nucleusof the inferior colliculus (ICc;
[25,26, review: 27��]).Paradoxically, the main components of
creation of facil-itatory delay-sensitivity in ICc are glycinergic
inputs[28,27��]. In addition, the ICc inherits a
delay-tunedinhibition from the intermediate nucleus of the
laterallemniscus (INLL), conveyed via an excitatory glutami-nergic
input [28–32]. Within the ICc, delay tuned neuronsare integrated in
the tonotopic representation and are notarranged according to CD
[33], and they also can be tunedto sound duration [34]. The
tectothalamic projectioncreates spatially discrete assemblies of
delay-tunedneurons in two regions of the rostral half of the
medialgeniculate body (MGB) that are organized according toharmonic
frequency bands (FM2, 3, 4). Furthermore,there is a crude
representation of characteristic delay inMGB [35, for further
references see 27��].
Thalamocortical projections feed three discrete rangingareas in
AC of P. parnellii. The FM-FM-area and the VFreceive overlapping
projections from rostral MGB derivedmainly from lateral parts,
whereas the DF receives inputfrom medial parts [36]. Since there
are massive cortico-thalamic backprojections, the cortex could also
imprint itschronotopic organization onto its main input structure.
Sofar, specific functional roles have not been assigned to
themultiple delay representations.
Figure 3 Legend Target range maps in different bat species.
Left: represent
position of auditory cortex. Right: detailed view of chronotopic
maps within
give direction of representation of decreasing echo delay. Black
arrows indi
that in E. fuscus and M. lucifugus, delay-sensitive neurons are
not arranged
Cortex data are from Schuller et al. [18], Suga [12],
Hechavarria et al. [23�], Ha
rouxi were kindly provided by D. Leipert, calls for M. lucifugus
by B. Fenton
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Emergent features within target distancemapsNeural processing to
create delay tuning in P. parnelliiappears largely complete at
subcortical levels. The sharp-ness of delay tuning (50% width) is
similar in IC, MGBand AC [15,26,35,37]. Furthermore, the range of
CDs issimilar in IC, MGB, and AC with an overrepresentation
ofdelays from 1 to 10 ms [15,26].
Cortical delay-tuned responses, on the other handhave certain
response features and show interactionsthat are not yet present at
lower levels and could havebeen implemented with the help of a
chronotopicgradient:� Among those are a higher specificity
regarding stimulus
type in P. parnellii for FM stimulus pairs and
lessresponsiveness to single FM components or to puretone stimuli
than in the IC and MGB [14,27��,37,38].However, in this respect
cortical delay-tuned neuronsin C. perspicillata are clearly less
specific and they allrespond vigorously to single pure tones
[39�].
� Mechanisms of lateral inhibition and excitatoryfeedback that
sharpen or shift response tuning areone of the major advantages of
a map, and could beused to provide dynamic plasticity of receptive
fieldsduring learning or arousal [40]. There is ampleevidence from
the work of Suga and colleagues onplasticity of neuronal tuning
both in tonotopic and intarget range sensitive cortical areas in P.
parnellii.They showed that a combination of widespread
lateralinhibition in the cortex and highly focused
excitatoryfeedback via projections to other cortical or
sub-cortical areas creates a self-organizing map [8��,41].Cortical
neurons within this map that code beha-viourally important stimuli,
can augment the activityof neurons with a similar, ‘matched’ CD in
the targetarea and also recruit additional neurons while activityof
unmatched neurons is reduced. For the intra-cortical interaction
between the 3 target distancemaps, this type of ‘egocentric
selection’ has beendemonstrated by local cortical electrical
activation[42–45]: The FM-FM area predominantly maintainsa strong
suppressive influence on unmatchedneurons in the other two areas
and on thecontralateral FM-FM area. This suppression canalso result
in a shift of the CD of the unmatchedneurons away from the CD of
the FM-FM neuron(centrifugal CD shift). In contrast, the DF and
VFareas have a mostly augmenting influence onmatched neurons in the
FM-FM area. This can
ative spectrograms of echolocation calls. Middle: brain overview
with the
auditory cortex. Target range computing areas are in blue, white
arrows
cate increasing characteristic frequency in tonotopic areas.
Please note
in a chrontopic map but are interspersed within the tonotopic
cortex.
gemann et al. [22��], Dear et al. [21], Wong and Shannon [19].
Calls for R.
, calls from E. fuscus by M. Gadziola.
Current Opinion in Neurobiology 2014, 24:68–75
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72 Neural maps
shift the CD of matched neurons closer to the CD ofthe DF or VF
neuron (centripetal CD shift). Thelatter could produce a focussing
on and sharpeningof tuning to short echo delays in the FM-FM
area,since the mapped delay range in DF and VF isrestricted to
shorter delays in comparison to the FM-FM area [see 8��].This form
of self-organizing feedback interaction is aquite powerful general
neuronal organization principleand is also found in the interaction
between cortex andICc and MGB [46,47]. In general, the dominance
ofcentrifugal plasticity could shape the selective
neuralrepresentation of a specific target distance and
producecontrast enhancement. Dominance of centripetalactions could
result in strong clustering and expandthe representation of a
selected specific targetdistance.
� In P. parnellii, P. quadridens, and C. perspicillata,
asubstantial proportion of cortical delay-tunedneurons, in
particular those responding to longerdelays at threshold have a
tilted receptive field thatcould allow a certain degree of target
tracking(Figure 2, [39�,23�]). When the bat approaches itstarget,
echo intensity increases due to decreasingtarget-range. As a
consequence, during the end stageof approach, only those neurons
with appropriatelytilted receptive field will continue to respond
tolouder echoes at shorter delays. In this respect tiltedreceptive
fields loose specificity in terms of staticobject distance but gain
specificity in terms ofresponding to echo series that are typical
for approachto target — and may facilitate target tracking. We
notethat some bat species reduce call intensity [48], andthen this
sort of tracking at the level of individualneurons would not work.
For P. parnellii tiltedresponse areas are present in the FM-FM area
butare not found in the IC [49�]. They could be generatedwithin the
topographic gradient of the map if there is alevel-dependent
asymmetry of input convergence orinput integration in cortical
neurons.
� Map topography could also provide a more effectivemeans to
exert local and delay-specific gain regulationby modulation through
local GABAergic interneuronsor external modulatory systems.
� Additional parameter representation: A 2D repres-entation of a
single parameter (echo delay) in principleallows arranging
additional axes orthogonal to the mapto represent/process other
features. In the FM-FM andDF areas of P. parnellii, the three
relevant frequencybands of the echo harmonics (FM2, 3, 4) are
separatedand projected orthogonal to the delay axis [14,15]. Sucha
harmonic dissociation is not found in P. quadridens orC.
perspicillata and in R. rouxi there are no relevantmultiple
harmonics in the echo.
� Chronotopic maps could also serve non-target relevantpurposes:
In P. parnellii, neurons in the FM-FM areanot only respond well to
FM pulse-echo pairs of
Current Opinion in Neurobiology 2014, 24:68–75
specific delay but also to the specific temporal syntax
ofsyllables within communication sounds [50,51].
Chronotopic maps as interface to spatial-memory,
decision-making, and motor-controlsystems?Chronotopic maps of
target distance that, depending onthe echolocation situation,
plastically adjust to mostrelevant input features (see above) could
also providean efficient interface to other cortical processing
systems.Completely unknown is the transfer of spatial infor-mation
from target distance maps to hippocampal placecells that in bats
have features comparable to those inrodents [52,53��].
A chronotopically organized target distance representa-tion
could provide an efficient interface to the motorsystem, in
particular since there are target-distancespecific behaviours. Most
notable is the switch fromlow call repetition rates during the
approach phase ofecholocation to high call repetition rates in the
finalphase shortly before the insect is caught. The wingcontrol
breaking behaviour close to obstacles (alarmhypothesis, [18]) is
also target-distance specific. Bothtypes of behaviour should be
triggerable by short echodelays, and the above mentioned
intracortical positivefeedback systems that enhance activity to
short echodelays may be especially efficient for inducing
thosebehaviours. There are also specific reactions to conspe-cifics
if they fly close by [54].
A chronotopic representation may also offer advantagesfor
efficient input from decision-making systems. Theneurons in the
FM-FM area that respond both tocall-echo pairs of specific delay
and to complex communi-cation signals may have input from auditory
regions offrontal cortex [55,56]. It is still to be tested if
frontal cortexcould initiate a switching between both processing
modesin the FM-FM area.
But how are bats without target-distancemaps coping?In two
insectivorous bat species that exclusively use FMecholocation
signals and that predominantly hunt in openuncluttered space,
target distance maps have not beendemonstrated. In E. fuscus
(Figure 3) delay-sensitiveneurons are clustered mainly between two
tonotopic areasand are interspersed with neurons sensitive to
single puretones. In M. lucifugus the cortical location of those
neuronsoverlaps with tonotopically arranged neurons. Theabsence of
a delay map in E. fuscus has inspired research-ers to develop an
alternative model for cortical repres-entation of target distance
and acoustic scenes based onensemble coding over a larger number of
neurons[20��,57,58��,59��]. It also has been demonstrated thatthe
population of cortical neurons tuned to echo-delaycould integrate
information from objects with different
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Target range maps in echolocating bats Kössl et al. 73
space-depths for the formation of acoustic images. Thelatter
mechanism can manage a quite powerful processingof realistic
echolocation call/echo sequences [59��] and itcould also be present
in the cortex of bat species that havea delay map [60]. Therefore,
at present there is still anopen discussion if delay maps are
strictly necessary forefficient extraction of spatial target
distance informationor if important features of such a processing
also could beobtained by other cortical mechanisms.
Innate cortical chronotopy in batsSharply tuned delay-sensitive
cortical neurons arealready present in neonate P. parnellii and C.
perspicil-lata, and their topography is comparable to those of
adultmaps [61��]. In particular the neurons tuned to shortecho
delay have receptive fields that are quite similar tothose of
adults. In this respect the delay-tuned dorsalauditory cortex
matures earlier than the tonotopicprimary auditory cortex [62]. The
establishment ofthose first basic maps of target distance takes
placewithout prior experience since the young bats do notyet
echolocate [63,64] and therefore the maps seem tobe hardwired in
early prenatal developmental stages. Ofcourse we expect that during
ongoing postnatal devel-opment the above described feedback
mechanismsexert a fine-tuning and adaptation of certain featuresof
delay-tuned neurons. However, basic implementa-tion of
target-distance sensitive neurons and maps isprobably of high
evolutionary value such that a prewir-ing that is genetically
determined takes place. It isnoteworthy that the a priori
implementation of activespace perception in bats has its complement
in passivespace perception: in young rodents, head-direction
cellsand hippocampal place cells are already implementedbefore
their first use [65,66].
ConclusionActive space perception by means of echo-delay
tunedneurons is essential for echolocating bats. In manyspecies,
these neurons are arranged in cortical mapsthat possess a rather
unique chronotopic neuronalrepresentation. Basic features of such
target-distancemaps are innate and most probably hardwired. This
apriori implementation of spatial perception emphasizestheir
behavioural relevance for bats. Importantly, oncetarget-distance
maps are established they seem to beconserved during evolution of
bat families and theywere implemented at least two times
independentlyin convergent evolution in old and new world
bats.However, the functional relevance of such maps is
stilldiscussed since there are other coding principles thatcould
extract echo delay information from auditoryscenes. In addition, an
ordered time representation onthe cortical surface could also be
exploited for extractingsignal features that are not related to
echolocation but tocommunication.
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Neural maps for target range in the auditory cortex of
echolocating batsIntroductionChronotopic target range maps in
different bat speciesGeneration of cortical chronotopyEmergent
features within target distance mapsChronotopic maps as interface
to spatial-memory, decision-making, and motor-control systems?But
how are bats without target-distance maps coping?Innate cortical
chronotopy in batsConclusionReferences and recommended reading