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In many mammals, upward-sweeping frequency-modulated (FM) sounds (up-chirps) evoke larger auditory brainstem responses than downward-sweeping sounds (down-chirps). To determine if similar effects occur in FM echolocating bats, auditory evoked responses (AERs) in big brown bats in response to up-chirps and down-chirps at different chirp durations and levels were recorded. Even though down-chirps are the biologically relevant stimulus for big brown bats, up-chirps typically evoked larger peaks in the AER, but with some exceptions at the shortest chirp durations. The up-chirp duration that produced the largest AERs and the greatest differences between up-chirps and down-chirps varied between individual bats and stimulus levels. Cross-covariance analyses using the entire AER waveform confirmed that amplitudes were typically larger to up-chirps than down-chirps at supra-threshold levels, with optimal durations around 0.5–1 ms. Changes in response latencies with stimulus levels were consistent with previous estimates of amplitude-latency trading. Latencies tended to decrease with increasing up-chirp duration and increase with increasing down-chirp duration. The effects of chirp direction on AER waveforms are generally consistent with those seen in other mammals but with small differences in response patterns that may reflect specializations for FM echolocation.

Little is known about the neural mechanisms that mediate differential action–selection responses to communication and echolocation calls in bats. For example, in the big brown bat, frequency modulated (FM) food-claiming communication calls closely resemble FM echolocation calls, which guide social and orienting behaviors, respectively. Using advanced signal processing methods, we identified fine differences in temporal structure of these natural sounds that appear key to auditory discrimination and behavioral decisions. We recorded extracellular potentials from single neurons in the midbrain inferior colliculus (IC) of passively listening animals, and compared responses to playbacks of acoustic signals used by bats for social communication and echolocation. We combined information obtained from spike number and spike triggered averages (STA) to reveal a robust classification of neuron selectivity for communication or echolocation calls. These data highlight the importance of temporal acoustic structure for differentiating echolocation and food-claiming social calls and point to general mechanisms of natural sound processing across species.

While approaching an object, echolocating bats decrease the amplitude of their vocalizations. This behavior is known as "echo-level compensation." Here, the activation pattern of the cortical FM-FM (frequency modulated) area of the mustached bat is assessed by using acoustic stimuli that correspond to sonar signals and their echoes emitted during echo-level compensation behavior. Activation maps were calculated from the delay response areas of 86 cortical neurons, and these maps were used to explore the topography of cortical activation during echolocation and its relation to the bats' cortical "chronotopy." Chronotopy predicts short echo-delays to be represented by rostral auditory cortex neurons while caudal neurons represent long echo-delays. The results show that a chronotopic activation of the cortex is evident only at loud pulse amplitudes [80-90 dB sound pressure level (SPL)]. In response to fainter pulse levels (60-70 dB SPL), as those produced as the animals zoom-in on targets, chronotopic activation of the cortex becomes less clear because units throughout the FM-FM area start firing, especially in response to short echo-delays. The fact that cortical activity is more widespread in response to combinations of short echo-delays and faint pulse amplitudes could represent an adaptation that enhances cortical activity in the late stages of echo-level compensation.

During echolocation, bats continuously perform audio-motor adjustments to optimize detection efficiency. It has been demonstrated that bats adjust the amplitude of their biosonar vocalizations (known as 'pulses') to stabilize the amplitude of the returning echo. Here, we investigated this echo-level compensation behaviour by swinging mustached bats on a pendulum towards a reflective surface. In such a situation, the bats lower the amplitude of their emitted pulses to maintain the amplitude of incoming echoes at a constant level as they approach a target. We report that cortical auditory neurons that encode target distance have receptive fields that are optimized for dealing with echo-level compensation. In most cortical delay-tuned neurons, the echo amplitude eliciting the maximum response matches the echo amplitudes measured from the bats' biosonar vocalizations while they are swung in a pendulum. In addition, neurons tuned to short target distances are maximally responsive to low pulse amplitudes while neurons tuned to long target distances respond maximally to high pulse amplitudes. Our results suggest that bats dynamically adjust biosonar pulse amplitude to match the encoding of target range and to keep the amplitude of the returning echo within the bounds of the cortical map of echo delays.

To navigate in the natural environment, animals must adapt their locomotion in response to environmental stimuli. The echolocating bat relies on auditory processing of echo returns to represent its surroundings. Recent studies have shown that echo flow patterns influence bat navigation, but the acoustic basis for flight path selection remains unknown. To investigate this problem, we released bats in a flight corridor with walls constructed of adjacent individual wooden poles, which returned cascades of echoes to the flying bat. We manipulated the spacing and echo strength of the poles comprising each corridor side, and predicted that bats would adapt their flight paths to deviate toward the corridor side returning weaker echo cascades. Our results show that the bat's trajectory through the corridor was not affected by the intensity of echo cascades. Instead, bats deviated toward the corridor wall with more sparsely spaced, highly reflective poles, suggesting that pole spacing, rather than echo intensity, influenced bat flight path selection. This result motivated investigation of the neural processing of echo cascades: We measured local evoked auditory responses in the bat inferior colliculus to echo playback recordings from corridor walls constructed of sparsely and densely spaced poles. We predicted that evoked neural responses would be discretely modulated by temporally distinct echoes recorded from the sparsely spaced pole corridor wall, but not by echoes from the more densely spaced corridor wall. The data confirm this prediction and suggest that the bat's temporal resolution of echo cascades may drive its flight behavior in the corridor.

Echolocating bats must process temporal streams of sonar sounds to represent objects along the range axis. Neuronal echo-delay tuning, the putative mechanism of sonar ranging, has been characterized in the inferior colliculus (IC) of the mustached bat, an insectivorous species that produces echolocation calls consisting of constant frequency and frequency modulated (FM) components, but not in species that use FM signals alone. This raises questions about the mechanisms that give rise to echo-delay tuning in insectivorous bats that use different signal designs. To investigate whether stimulus context may account for species differences in echo-delay selectivity, we characterized single-unit responses in the IC of awake passively listening FM bats, Eptesicus fuscus, to broadcasts of natural sonar call-echo sequences, which contained dynamic changes in signal duration, interval, spectrotemporal structure, and echo-delay. In E. fuscus, neural selectivity to call-echo delay emerges in a population of IC neurons when stimulated with call-echo pairs presented at intervals mimicking those in a natural sonar sequence. To determine whether echo-delay selectivity also depends on the spectrotemporal features of individual sounds within natural sonar sequences, we studied responses to computer-generated echolocation signals that controlled for call interval, duration, bandwidth, sweep rate, and echo-delay. A subpopulation of IC neurons responded selectively to the combination of the spectrotemporal structure of natural call-echo pairs and their temporal patterning within a dynamic sonar sequence. These new findings suggest that the FM bat’s fine control over biosonar signal parameters may modulate IC neuronal selectivity to the dimension of echo-delay. NEW & NOTEWORTHY Echolocating bats perform precise auditory temporal computations to estimate their distance to objects. Here, we report that response selectivity of neurons in the inferior colliculus of a frequency modulated bat to call-echo delay, or target range tuning, depends on the temporal patterning and spectrotemporal features of sound elements in a natural echolocation sequence. We suggest that echo responses to objects at different distances are gated by the bat’s active control over the spectrotemporal patterning of its sonar emissions.

During echolocation, bats estimate distance to avoid obstacles and capture moving prey. The primary distance cue is the delay between the bat's emitted echolocation pulse and the return of an echo. In the bat's auditory system, echo delay-tuned neurons that only respond to pulse-echo pairs having a specific echo delay serve target distance calculation. Accurate prey localization should benefit from the spike precision in such neurons. Here we show that delay-tuned neurons in the inferior colliculus of the mustached bat respond with higher temporal precision, shorter latency and shorter response duration than those of the auditory cortex. Based on these characteristics, we suggest that collicular neurons are best suited for a fast and accurate response that could lead to fast behavioral reactions while cortical neurons, with coarser temporal precision and longer latencies and response durations could be more appropriate for integrating acoustic information over time. The latter could be important for the formation of biosonar images.

In this study, we evaluate the potential of the heterodyne system for the acoustic identification of bat species from Mormoopidae in Cuba. The heterodyne transformation of the echolocation calls of the three mormoopid species of Pteronotus (P. macleayii, P. quadridens and P. parnellii) was initially analyzed by setting the frequency of the heterodyne detector (f tuned) 5 kHz above and below the constant frequency value of the second harmonic, respectively. We then studied the feasibility for the identification of several Pteronotus species with single ftuned values. The heterodyne transformation of calls from the mormoopid Mormoops blainvillii and four Cuban phyllostomid bats was studied by selecting frequency values contained in the calls of each of the species under study. We showed that, by selecting the appropriate f tuned, the Pteronotus species could be accurately identified based on the spectral signatures of their heterodyned calls. Frequency modulated (FM) bats presented very similar he...

Temporal analysis of sound is fundamental to auditory processing throughout the animal kingdom. Echolocating bats are powerful models for investigating the underlying mechanisms of auditory temporal processing, as they show microsecond precision in discriminating the timing of acoustic events. However, the neural basis for microsecond auditory discrimination in bats has eluded researchers for decades. Combining extracellular recordings in the midbrain inferior colliculus (IC) and mathematical modeling, we show that microsecond precision in registering stimulus events emerges from synchronous neural firing, revealed through low-latency variability of stimulus-evoked extracellular field potentials (EFPs, 200–600 Hz). The temporal precision of the EFP increases with the number of neurons firing in synchrony. Moreover, there is a functional relationship between the temporal precision of the EFP and the spectrotemporal features of the echolocation calls. In addition, EFP can measure the time difference of simulated echolocation call–echo pairs with microsecond precision. We propose that synchronous firing of populations of neurons operates in diverse species to support temporal analysis for auditory localization and complex sound processing., Author summary We routinely rely on a stopwatch to precisely measure the time it takes for an athlete to reach the finish line. Without the assistance of such a timing device, our measurement of elapsed time becomes imprecise. By contrast, some animals, such as echolocating bats, naturally perform timing tasks with remarkable precision. Behavioral research has shown that echolocating bats can estimate the elapsed time between sonar cries and echo returns with a precision in the range of microseconds. However, the neural basis for such microsecond precision has remained a puzzle to scientists. Combining extracellular recordings in the bat’s inferior colliculus (IC)—a midbrain nucleus of the auditory pathway—and mathematical modeling, we show that microsecond precision in registering stimulus events emerges from synchronous neural firing. Our recordings revealed a low-latency variability of stimulus-evoked extracellular field potentials (EFPs), which, according to our mathematical modeling, was determined by the number of firing neurons and their synchrony. Moreover, the acoustic features of echolocation calls, such as signal duration and bandwidth, which the bat dynamically modulates during prey capture, also modulate the precision of EFPs. These findings have broad implications for understanding temporal analysis of acoustic signals in a wide range of auditory behaviors across the animal kingdom.

In the auditory system, tuning to sound level appears in the form of non-monotonic response-level functions that depict the response of a neuron to changing sound levels. Neurons with non-monotonic response-level functions respond best to a particular sound pressure level (defined as "best level" or level evoking the maximum response). We performed a comparative study on the location and basic functional organization of the auditory cortex in the gleaning bat, Macrotus waterhousii, and the aerial-hawking bat, Molossus molossus. Here, we describe the response-level function of cortical units in these two species. In the auditory cortices of M. waterhousii and M. molossus, the characteristic frequency of the units increased from caudal to rostral. In M. waterhousii, there was an even distribution of characteristic frequencies while in M. molossus there was an overrepresentation of frequencies present within echolocation pulses. In both species, most of the units showed best levels in a narrow range, without an evident topography in the amplitopic organization, as described in other species. During flight, bats decrease the intensity of their emitted pulses when they approach a prey item or an obstacle resulting in maintenance of perceived echo intensity. Narrow level tuning likely contributes to the extraction of echo amplitudes facilitating echo-intensity compensation. For aerial-hawking bats, like M. molossus, receiving echoes within the optimal sensitivity range can help the bats to sustain consistent analysis of successive echoes without distortions of perception caused by changes in amplitude.

Echolocation in bats requires a precise temporal processing of complex signals. This processing of time includes the encoding of echo-delay, which gives an estimation of target distance, and sound duration, which is considered to be important for own sound or echo recognition. In this study, we report that delay-tuned neurons in the inferior colliculus of the mustached bat (Pteronotus parnellii) are also tuned to sound duration. Collicular delay-tuned neurons showed three types of duration tuning: short-pass (12 of 64), band-pass (16 of 64), and long-pass (17 of 64). The remaining 19 delay-tuned neurons are not selective for sound duration. All short-pass and 10 band-pass neurons' characteristic delays were similar to characteristic duration. In six band-pass neurons, characteristic delay was different from characteristic duration. Neurons processing unmatched delay and durations could be participating in complex kinds of processing where the same neuron has different functions depending on the activated neural network.

The mechanisms by which the mammalian brain copes with information from natural vocalization streams remain poorly understood. This article shows that in highly vocal animals, such as the bat species Carollia perspicillata, the spike activity of auditory cortex neurons does not track the temporal information flow enclosed in fast time-varying vocalization streams emitted by conspecifics. For example, leading syllables of so-called distress sequences (produced by bats subjected to duress) suppress cortical spiking to lagging syllables. Local fields potentials (LFPs) recorded simultaneously to cortical spiking evoked by distress sequences carry multiplexed information, with response suppression occurring in low frequency LFPs (i.e. 2–15 Hz) and steady-state LFPs occurring at frequencies that match the rate of energy fluctuations in the incoming sound streams (i.e. >50 Hz). Such steady-state LFPs could reflect underlying synaptic activity that does not necessarily lead to cortical spiking in response to natural fast time-varying vocal sequences.

In the cochlea of the mustached bat, cochlear resonance produces extremely sharp frequency tuning to the dominant frequency of the echolocation calls, around 61 kHz. Such high frequency resolution in the cochlea is accomplished at the expense of losing temporal resolution because of cochlear ringing, an effect that is observable not only in the cochlea but also in the cochlear nucleus. In the midbrain, the duration of sounds is thought to be analyzed by duration-tuned neurons, which are selective to both stimulus duration and frequency. We recorded from 57 DTNs in the auditory midbrain of the mustached bat to assess if a spectral-temporal trade-off is present. Such spectral-temporal trade-off is known to occur as sharp tuning in the frequency domain which results in poorer resolution in the time domain, and vice versa. We found that a specialized sub-population of midbrain DTNs tuned to the bat’s mechanical cochlear resonance frequency escape the cochlear spectral-temporal trade-off. We also show evidence that points towards an underlying neuronal inhibition that appears to be specific only at the resonance frequency.

Distress vocalizations (also known as alarm or screams) are an important component of the vocal repertoire of a number of animal species, including bats, humans, monkeys and birds, among others. Although the behavioral relevance of distress vocalizations is undeniable, at present, little is known about the rules that govern vocalization production when in alarmful situations. In this article, we show that when distressed, bats of the species Carollia perspicillata produce repetitive vocalization sequences in which consecutive syllables are likely to be similar to one another regarding their physical attributes. The uttered distress syllables are broadband (12-73 kHz) with most of their energy focussing at 23 kHz. Distress syllables are short (~4 ms), their average sound pressure level is close to 70 dB SPL, and they are produced at high repetition rates (every 14 ms). We discuss that, because of their physical attributes, bat distress vocalizations could serve a dual purpose: (1) advertising threatful situations to conspecifics, and (2) informing the threatener that the bats are ready to defend themselves. We also discuss possible advantages of advertising danger/discomfort using repetitive utterances, a calling strategy that appears to be ubiquitous across the animal kingdom.

One role of the inferior colliculus (IC) in bats is to create neuronal delay-tuning, which is used for the estimation of target distance in the echolocating bat's auditory system. In this study, we describe response properties of IC delay-tuned neurons of the mustached bat (Pteronotus parnellii) and compare it with those of delay-tuned neurons of the auditory cortex (AC). We also address the question if frequency content of the stimulus (pure-tone (PT) or frequency-modulated (FM) pairs stimulation) affects combination-sensitive interaction in the same neuron. Sharpness and sensitivity of delay-tuned neurons in the IC are similar to those described in the AC. However, in contrast to cortical responses, in collicular neurons the delay at which the neurons show the maximum response does not change with changes in echo level. This tolerance to changes in the echo level seems to be a property of collicular delay-tuned neurons, which is modified along the ascending auditory pathway. In the IC we found neurons that showed a facilitated delay-tuned response when stimulated with FM components and did not show any delay-tuning with PT stimulation. This result suggests that not only is echo delay-tuning generated in the IC but also its FM-specificity observed in the cortex could be created to some extent in the IC and then topographically organized at higher levels.

Echolocation signals were recorded from the Macleay's bat (Pteronotus macleayii) while hunting for insects in the field. Search, approach and terminal phases were identified in the foraging activity of the species. During search phase, P. macleayii emitted calls consisting of a short CF component followed by a downward FM sweep (sCF-FM), typical of the small Pteronotus species. In addition, FM-sCF calls were recorded. In search flight some sequences consisted only of sCF-FM calls while others consisted only of FM-sCF calls. Most sequences, however, combined both call designs. Based on this and previous studies we suggest that sCF-FM and FM-sCF calls will characterize the vocal repertoire of each of the small Pteronotus species. We discuss the relevance of our results for acoustic identification of P. macleayii and the other small Pteronotus in the field.

Echolocation calls emitted by the 4 species of Cuban mormoopid bats were compared to determine vocal signatures that enable identification of each species in the field during their evening exodus. Echolocation calls produced by Mormoops blainvilli are downward frequency-modulated (FM) signals in the range of 68.4– 52.5 kHz. Echolocation calls emitted by Pteronotus macleayii and P. quadridens have a similar design consisting of a short constant-frequency (CF) segment followed by a downward FM segment. The CF segment was at 70.0 kHz in calls from P. macleayii, and at 83.3 kHz in calls from P. quadridens. Echolocation calls from P. parnellii consist of a long CF segment, which is preceded by a short initial upward sweep and followed by a downward FM terminal sweep. The CF value of the 2nd harmonic was a good parameter for species identification. The features of the echolocation calls of each of the species were used to identify them during the evening exodus from 2 Cuban caves.

We studied the echolocation calls emitted by Phyllops falcatus (Chiroptera: Phyllostomidae) during foraging, in the field and in the lab. Calls emitted in free flight, in a more or less uncluttered situation, were about 4.5 ms (up to 5.3 ms) long and characterized by a sweep of the first harmonic (= fundamental) from ca. 73 kHz down to about 23 kHz, which is unusually large for phyllostomid bats. A less intense second harmonic was always present. The intervals between pulses varied between 55 and 170 ms with a mean of about 110 ms. During approach to bushes or trees (or during flight in confined space between bushes), or in the flight room, calls became shorter (ca. 2 ms) and more energy was allocated to the second harmonic, sometimes also a third harmonic appeared. During approach to a fruit calls were further shortened (about 1 ms or less), and call frequency increased to about 5 calls/100 ms, calls often being grouped. The large bandwidth of the first harmonic separates Phyllops from all other Cuban bat species and allows identification in the field.

We studied the echolocation behaviour of Nycticeius cubanus in the field in western Cuba. During hunting, N. cubanus search for insects emitting cries that sweep from 80 to 40 kHz in 4 to 12 ms. Search call characteristics correlate with the clutter structure of the hunting areas. Bats hunting in an uncluttered space broadcast longer and narrower signals, while bats hunting in cluttered space broadcast shorter and broadband signals. Longer calls were emitted with longer intervals while the duty cycle was kept below 15 % during search and approach phases. The call's minimal frequency remained about 43 kHz showing variation coefficients of less than 3%. As a consequence, bandwidth correlates positively with the maximal frequency. Calls emitted by different sympatric individuals are accurately classified by sender using a discriminant function analysis, suggesting vocal signatures in N. cubanus. The statistical analysis of several passes of calls broadcast during the hunting activity of a single ind...

Echolocation calls were recorded from Pteronotus quadridens flying in the field and in an enclosed space. In the field, search calls contained 1 or 2 harmonics. Patterns of call design show a segment of quasi–constant frequency (QCF2nd-harmonic at 81–84 kHz), followed by a downward frequency-modulated (FM) component. The 2nd harmonic was always more intense than the 1st. Search, approach, and terminal phases of calls were described during hunting sequences of P. quadridens. The transition between call phases was characterized by monotonic variations in some acoustic parameters, including a decrease in call duration and an increase in repetition rate, bandwidth, and slope of the FM component. We also analyzed calls emitted by bats flying in confined spaces that consistently contained 3 harmonics, of which the 2nd harmonic contained the greatest energy. The values of call duration were shorter and bandwidth was higher than values characterizing calls emitted during the search phase in the field.

We investigated response selectivity of single neurons in the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus, to acoustic elements embedded in the natural temporal patterning of dynamic frequency modulated (FM) echolocation sequences. Acoustic stimuli consisted of species-specific sonar sequences, with natural dynamic spectro-temporal features, containing both bat-emitted FM pulses and echoes from a moving target. Roughly 50% of sampled IC neurons showed responses to a restricted subset of stimulus elements in the natural sonar sequence and selectivity to the time delay between pulses and echoes, the bat’s cue for target distance. Importantly, response selectivity emerged only when stimulus elements were embedded in natural sequences and was absent when the same neurons were stimulated with isolated pulse-echo pairs presented randomly at 300 ms stimulus intervals. These data provide compelling evidence that natural and dynamic sound sequences are necessary to evoke selectivity to pulse-ec...

It has been reported previously that in the inferior colliculus of the bat Molossus molossus, neuronal duration tuning is ambiguous because the tuning type of the neurons dramatically changes with the sound level. In the present study, duration tuning was examined in the auditory cortex of M. molossus to describe if it is as ambiguous as the collicular tuning. From a population of 174 cortical 104 (60 %) neurons did not show duration selectivity (all-pass). Around 5 % (9 units) responded preferentially to stimuli having longer durations showing long-pass duration response functions, 35 (20 %) responded to a narrow range of stimulus durations showing band-pass duration response functions, 24 (14 %) responded most strongly to short stimulus durations showing short-pass duration response functions and two neurons (1 %) responded best to two different stimulus durations showing a two-peaked duration–response function. The majority of neurons showing short- (16 out of 24) and band-pass (24 out 35) selectivity displayed “O-shaped” duration response areas. In contrast to the inferior colliculus, duration tuning in the auditory cortex of M. molossus appears level tolerant. That is, the type of duration selectivity and the stimulus duration eliciting the maximum response were unaffected by changing sound level.

Echolocating bats use the time from biosonar pulse emission to the arrival of echo (defined as echo delay) to calculate the space depth of targets. In the dorsal auditory cortex of several species, neurons that encode increasing echo delays are organized rostrocaudally in a topographic arrangement defined as chronotopy. Precise chronotopy could be important for precise target-distance computations. Here we show that in the cortex of three echolocating bat species (Pteronotus quadridens, Pteronotus parnellii and Carollia perspicillata), chronotopy is not precise but blurry. In all three species, neurons throughout the chronotopic map are driven by short echo delays that indicate the presence of close targets and the robustness of map organization depends on the parameter of the receptive field used to characterize neuronal tuning. The timing of cortical responses (latency and duration) provides a binding code that could be important for assembling acoustic scenes using echo delay information from objects with different space depths.

Echolocating bats use the time elapsed from biosonar pulse emission to the arrival of echo (defined as echo-delay) to assess target-distance. Target-distance is represented in the brain by delay-tuned neurons that are classified as either “heteroharmonic” or “homoharmormic.” Heteroharmonic neurons respond more strongly to pulse-echo pairs in which the timing of the pulse is given by the fundamental biosonar harmonic while the timing of echoes is provided by one (or several) of the higher order harmonics. On the other hand, homoharmonic neurons are tuned to the echo delay between similar harmonics in the emitted pulse and echo. It is generally accepted that heteroharmonic computations are advantageous over homoharmonic computations; i.e., heteroharmonic neurons receive information from call and echo in different frequency-bands which helps to avoid jamming between pulse and echo signals. Heteroharmonic neurons have been found in two species of the family Mormoopidae (Pteronotus parnellii and Pteronotus quadridens) and in Rhinolophus rouxi. Recently, it was proposed that heteroharmonic target-range computations are a primitive feature of the genus Pteronotus that was preserved in the evolution of the genus. Here, we review recent findings on the evolution of echolocation in Mormoopidae, and try to link those findings to the evolution of the heteroharmonic computation strategy (HtHCS). We stress the hypothesis that the ability to perform heteroharmonic computations evolved separately from the ability of using long constant-frequency echolocation calls, high duty cycle echolocation, and Doppler Shift Compensation. Also, we present the idea that heteroharmonic computations might have been of advantage for categorizing prey size, hunting eared insects, and living in large conspecific colonies. We make five testable predictions that might help future investigations to clarify the evolution of the heteroharmonic echolocation in Mormoopidae and other families.

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.

Delay tuning was studied in the auditory cortex of Pteronotus quadridens. All the 136 delay-tuned units that were studied responded strongly to heteroharmonic pulse-echo pairs presented at specific delays. In the heteroharmonic pairs, the first sonar call harmonic marks the timing of pulse emission while one of the higher harmonics (second or third) indicates the timing of the echo. Delay-tuned units are organized chronotopically along a rostrocaudal axis according to their characteristic delay. There is no obvious indication of multiple cortical axes specialized in the processing of different harmonic combinations of pulse and echo. Results of this study serve for a straight comparison of cortical delay-tuning between P. quadridens and the well-studied mustached bat, Pteronotus parnellii. These two species stem from the most recent and most basal nodes in the Pteronotus lineage, respectively. P. quadridens and P. parnellii use comparable heteroharmonic target-range computation strategies even though they do not use biosonar calls of a similar design. P. quadridens uses short constant-frequency (CF)/frequency-modulated (FM) echolocation calls, while P. parnellii uses long CF/FM calls. The ability to perform “heteroharmonic” target-range computations might be an ancestral neuronal specialization of the genus Pteronotus that was subjected to positive Darwinian selection in the evolution.

Neuronal computation of object distance from echo delay is an essential task that echolocating bats must master for spatial orientation and the capture of prey. In the dorsal auditory cortex of bats, neurons specifically respond to combinations of short frequency-modulated components of emitted call and delayed echo. These delay-tuned neurons are thought to serve in target range calculation. It is unknown whether neuronal correlates of active space perception are established by experience-dependent plasticity or by innate mechanisms. Here we demonstrate that in the first postnatal week, before onset of echolocation and flight, dorsal auditory cortex already contains functional circuits that calculate distance from the temporal separation of a simulated pulse and echo. This innate cortical implementation of a purely computational processing mechanism for sonar ranging should enhance survival of juvenile bats when they first engage in active echolocation behaviour and flight.

We studied duration tuning in neurons of the inferior colliculus (IC) of the mustached bat. Duration-tuned neurons in the IC of the mustached bat fall into three main types: short (16 of 136), band (34 of 136), and long (29 of 136) pass. The remaining 51 neurons showed no selectivity for the duration of sounds. The distribution of best durations was double peaked with maxima around 3 and 17 ms, which correlate with the duration of the short frequency-modulated (FM) and the long constant-frequency (CF) signals emitted by Pteronotus parnellii. Since there are no individual neurons with a double-peaked duration response profile, both types of temporal processing seem to be well segregated in the IC. Most short- and band-pass units with best frequency in the CF2 range responded to best durations > 9 ms (66%, 18 of 27 units). However, there is no evidence for a bias toward longer durations as there is for neurons tuned to the frequency range of the FM component of the third harmonic, where 83% (10 of 12 neurons) showed best durations longer than 9 ms. In most duration-tuned neurons, response areas as a function of stimulus duration and intensity showed either V or U shape, with duration tuning retained across the range of sound levels tested. Duration tuning was affected by changes in sound pressure level in only six neurons. In all duration-tuned neurons, latencies measured at the best duration were longer than best durations, suggesting that behavioral decisions based on analysis of the duration of the pulses would not be expected to be complete until well after the stimulus has occurred.

Frequency tuning, temporal response pattern and latency properties of inferior colliculus neurons were investigated in the big fruit-eating bat, Artibeus jamaicensis. Neurons having best frequencies between 48–72 kHz and between 24–32 kHz are overrepresented. The inferior colliculus neurons had either phasic (consisting in only one response cycle at all stimulus intensities) or long-lasting oscillatory responses (consisting of multiple response cycles). Seventeen percent of neurons displayed paradoxical latency shift, i.e. their response latency increased with increasing sound level. Three types of paradoxical latency shift were found: (1) stable, that does not depend on sound duration, (2) duration-dependent, that grows with increasing sound duration, and (3) progressive, whose magnitude increases with increasing sound level. The temporal properties of paradoxical latency shift neurons compare well with those of neurons having long-lasting oscillatory responses, i.e. median inter-spike intervals and paradoxical latency shift below 6 ms are overrepresented. In addition, oscillatory and paradoxical latency shift neurons behave similarly when tested with tones of different durations. Temporal properties of oscillation and PLS found in the IC of fruit-eating bats are similar to those found in the IC of insectivorous bats using downward frequency-modulated echolocation calls.

We recorded the echolocation behavior of the molossid bat Mormopterus minutus, a species that uses a plastic call inventory. During its foraging activity, M. minutus searches for insects emitting rather long and narrow-band echolocation calls. Search call design however, can vary noticeably even in a continuous foraging pass. While echolocating in different flying conditions M. minutus uses several other call designs such as short CF, QCF, FM/QCF, FM and multi-harmonic FM, with or without harmonic overlap, and QCF/FM. Call plasticity characterizes most echolocation sequences, particularly in bats flying in open spaces. Call variation was also influenced by the presence of conspecifics. In those sequences containing echolocation calls from more than one bat, signals from different individuals were reliably identified. In contrast to other small molossids, the call designs in the echolocation inventory of M. minutus show a high level of plasticity. Our results suggest that M. minutus has combined the advantages of emitting several call designs, as shown by molossids, with the advantages of manipulating one signal design as shown by vespertilionids within the same sonar inventory.

The extent of the auditory cortex in the bat Molossus molossus was electrophysiologically investigated. Best frequencies and minimum thresholds of neural tuning curves were analyzed to define the topography of the auditory cortex. The auditory cortex encompasses an average cortical surface area of 5 mm2. Characteristic frequencies are tonotopically organized with low frequencies being represented caudally and high frequencies rostrally. However, a large interindividual variability in the tonotopic organization was found. In most animals, the caudal 50% was tonotopically organized. More anterior, a variable area was found. A distinct field with reversed topography was not consistently found. Within the demarcated auditory cortex, frequencies of 30–40 kHz, which correspond to the frequency range of search calls emitted during hunting, are overrepresented, occupying 49% of the auditory cortex surface. High minimum thresholds >50 dB SPL were found in a narrow dorsal narrow area. Neurons with multipeaked tuning curves (20%) preferentially were located in the dorsal part of the auditory cortex. In accordance with studies in other bat species, the auditory cortex of M. molossus is highly sensitive to the dominant frequencies of biosonar search calls.

Unlike any other foraging phyllostomid bat studied to date, Poey’s flower bats (Phyllonycteris poeyi-Phyllostomidae) emit relatively long (up to 7.2 ms), intense, single-harmonic echolocation calls. These calls are readily detectable at distances of at least 15 m. Furthermore, the echolocation calls contain only the first harmonic, which is usually filtered out in the vocal tract of phyllostomids. The foraging echolocation calls of P. poeyi are more like search-phase echolocation calls of sympatric aerial-feeding bats (Molossidae, Vespertilionidae, Mormoopidae). Intense, long, narrowband, single-harmonic echolocation calls focus acoustic energy maximizing range and favoring detection, which may be particularly important for cruising bats, like P. poeyi, when flying in the open. Flying in enclosed spaces, P. poeyi emit short, low-intensity, frequency-modulated, multiharmonic echolocation calls typical of other phyllostomids. This is the first report of a phyllostomid species emitting long, intense, single-harmonic echolocation calls with most energy in the first harmonic.

Behavioral audiograms of Artibeus jamaicensis and Eptesicus fuscus are characterized by two threshold minima separated by a threshold maximum at 40 kHz, for A. jamaicensis , and 45 kHz, for E. fuscus [Koay, G., Heffner, H.E., Heffner R.S., 1997. Audiogram of the big brown bat ( Eptesicus fuscus ). Hear. Res. 105, 202–210; Heffner, R.S., Koay, G., Heffner H.E., 2003. Hearing in American leaf-nosed bats. III: Artibeus jamaicensis . Hear. Res. 184, 113–122.]. To investigate whether these characteristics are due to cochlear properties, we recorded distortion product otoacooustic emissions (DPOAEs) and calculated DPOAE threshold curves. We found that in both species cochlear sensitivity, assessed by DPOAE recordings, does not show local threshold maxima. The DPOAE threshold curve calculated for A. jamaicensis reveals a broadly tuned minimum for frequencies between 20 and 50 kHz and the threshold curve of E. fuscus shows a broad sensitive area for frequencies between 15 and 60 kHz. In none of the two species any pronounced threshold irregularities were found. The characteristic pattern of a threshold maximum followed by a minimum observed in behavioral studies seems to be shaped by transfer characteristics of the outer ear and/or neuronal processing in the ascending auditory pathway rather than by cochlear mechanics.

While searching for prey, Molossus molossus broadcasts narrow-band calls of 11.42 ms organized in pairs of pulses that alternate in frequency. The first signal of the pair is at 34.5 kHz, the second at 39.6 kHz. Pairs of calls with changing frequencies were only emitted when the interpulse intervals were below 200 ms. Maximum duty cycles during search phase are close to 20%. Frequency alternation of search calls is interpreted as a mechanism for increasing duty cycle and thus the temporal continuity of scanning, as well as increasing the detection range. A neurophysiological correlate for the processing of search calls was found in the inferior colliculus. 64% of neurons respond to frequencies in the 30- to 40-kHz range and only in this frequency range were closed tuning curves found for levels below 40 dB SPL. In addition, 15% of the neurons have double-tuned frequency-threshold curves with best thresholds at 34 and 39 kHz. Differing from observations in other bats, approach calls of M. molossus are longer and of higher frequencies than search calls. Close to the roost, the call frequency is increased to 45.0-49.8 kHz and, in addition, extremely broadband signals are emitted. This demonstrates high plasticity of call design.