Descending projections to the auditory midbrain: evolutionary considerations.

The mammalian inferior colliculus (IC) is massively innervated by multiple descending projection systems. In addition to a large projection from the auditory cortex (AC) primarily targeting the non-lemniscal portions of the IC, there are less well-characterized projections from non-auditory regions of the cortex, amygdala, posterior thalamus and the brachium of the IC. By comparison, the frog auditory midbrain, known as the torus semicircularis, is a large auditory integration center that also receives descending input, but primarily from the posterior thalamus and without a projection from a putative cortical homolog: the dorsal pallium. Although descending projections have been implicated in many types of behaviors, a unified understanding of their function has not yet emerged. Here, we take a comparative approach to understanding the various top-down modulators of the IC to gain insights into their functions. One key question that we identify is whether thalamotectal projections in mammals and amphibians are homologous and whether they interact with evolutionarily more newly derived projections from the cerebral cortex. We also consider the behavioral significance of these descending pathways, given anurans' ability to navigate complex acoustic landscapes without the benefit of a corticocollicular projection. Finally, we suggest experimental approaches to answer these questions.

The prefrontal cortex of the Mexican free-tailed bat is more selective to communication calls than primary auditory cortex.

In this study, we examined the auditory responses of a prefrontal area, the frontal auditory field (FAF), of an echolocating bat (Tadarida brasiliensis) and presented a comparative analysis of the neuronal response properties between the FAF and the primary auditory cortex (A1). We compared single-unit responses from the A1 and the FAF elicited by pure tones, downward frequency-modulated sweeps (dFMs), and species-specific vocalizations. Unlike the A1, FAFs were not frequency tuned. However, progressive increases in dFM sweep rate elicited a systematic increase of response precision, a phenomenon that does not take place in the A1. Call selectivity was higher in the FAF versus A1. We calculated the neuronal spectrotemporal receptive fields (STRFs) and spike-triggered averages (STAs) to predict responses to the communication calls and provide an explanation for the differences in call selectivity between the FAF and A1. In the A1, we found a high correlation between predicted and evoked responses. However, we did not generate reasonable STRFs in the FAF, and the prediction based on the STAs showed lower correlation coefficient than that of the A1. This suggests nonlinear response properties in the FAF that are stronger than the linear response properties in the A1. Stimulating with a call sequence increased call selectivity in the A1, but it remained unchanged in the FAF. These data are consistent with a role for the FAF in assessing distinctive acoustic features downstream of A1, similar to the role proposed for primate ventrolateral prefrontal cortex.NEW & NOTEWORTHY In this study, we examined the neuronal responses of a frontal cortical area in an echolocating bat to behaviorally relevant acoustic stimuli and compared them with those in the primary auditory cortex (A1). In contrast to the A1, neurons in the bat frontal auditory field are not frequency tuned but showed a higher selectivity for social signals such as communication calls. The results presented here indicate that the frontal auditory field may represent an additional processing center for behaviorally relevant sounds.

Faster Repetition Rate Sharpens the Cortical Representation of Echo Streams in Echolocating Bats.

There is consensus that primary auditory cortex (A1) utilizes a combination of rate codes and temporally precise population codes to represent discreet auditory objects. During the response to auditory streams, forward suppression constrains cortical rate coding strategies, but it may also be well positioned to enhance temporal coding strategies that rely on synchronized firing across neural ensembles. Here, we exploited the rapid temporal dynamics of bat echolocation to investigate how forward suppression modulates the cortical ensemble representation of complex acoustic signals embedded in echo streams. We recorded from auditory cortex of anesthetized free-tailed bats while stimulating the auditory system with naturalistic biosonar pulse-echo sequences covering a range of pulse emission rates. As expected, increasing pulse repetition rate significantly reduced the number of spikes per echo stimulus, but it also increased spike timing precision and doubled the information gain. This increased spike-timing precision translated into more robust inter-neuronal synchronization patterns with >10-dB higher signal-to-noise ratios (SNRs) at the ensemble level. We propose that forward suppression dynamically mediates a trade-off between the sensitive detection of isolated sounds versus precise spatiotemporal encoding of ongoing sound sequences in auditory cortex.

Temporal coding of echo spectral shape in the bat auditory cortex.

Echolocating bats rely upon spectral interference patterns in echoes to reconstruct fine details of a reflecting object's shape. However, the acoustic modulations required to do this are extremely brief, raising questions about how their auditory cortex encodes and processes such rapid and fine spectrotemporal details. Here, we tested the hypothesis that biosonar target shape representation in the primary auditory cortex (A1) is more reliably encoded by changes in spike timing (latency) than spike rates and that latency is sufficiently precise to support a synchronization-based ensemble representation of this critical auditory object feature space. To test this, we measured how the spatiotemporal activation patterns of A1 changed when naturalistic spectral notches were inserted into echo mimic stimuli. Neurons tuned to notch frequencies were predicted to exhibit longer latencies and lower mean firing rates due to lower signal amplitudes at their preferred frequencies, and both were found to occur. Comparative analyses confirmed that significantly more information was recoverable from changes in spike times relative to concurrent changes in spike rates. With this data, we reconstructed spatiotemporal activation maps of A1 and estimated the level of emerging neuronal spike synchrony between cortical neurons tuned to different frequencies. The results support existing computational models, indicating that spectral interference patterns may be efficiently encoded by a cascading tonotopic sequence of neural synchronization patterns within an ensemble of network activity that relates to the physical features of the reflecting object surface.

Functional organization of the primary auditory cortex of the free-tailed bat Tadarida brasiliensis.

The Mexican free-tailed bat, Tadarida brasiliensis, is a fast-flying bat that hunts by biosonar at high altitudes in open space. The auditory periphery and ascending auditory pathways have been described in great detail for this species, but nothing is yet known about its auditory cortex. Here we describe the topographical organization of response properties in the primary auditory cortex (AC) of the Mexican free-tailed bat with emphasis on the sensitivity for FM sweeps and echo-delay tuning. Responses of 716 units to pure tones and of 373 units to FM sweeps and FM-FM pairs were recorded extracellularly using multielectrode arrays in anesthetized bats. A general tonotopy was confirmed with low frequencies represented caudally and high frequencies represented rostrally. Characteristic frequencies (CF) ranged from 15 to 70 kHz, and fifty percent of CFs fell between 20 and 30 kHz, reflecting a hyper-representation of a bandwidth corresponding to search-phase echolocation pulses. Most units showed a stronger response to downward rather than upward FM sweeps and forty percent of the neurons interspersed throughout AC (150/371) showed echo-delay sensitivity to FM-FM pairs. Overall, the results illustrate that the free-tailed bat auditory cortex is organized similarly to that of other FM-type insectivorous bats.

Neural Response Selectivity to Natural Sounds in the Bat Midbrain.

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.

Laminar Organization of FM Direction Selectivity in the Primary Auditory Cortex of the Free-Tailed Bat.

We studied the columnar and layer-specific response properties of neurons in the primary auditory cortex (A1) of six (four females, two males) anesthetized free-tailed bats, Tadaridabrasiliensis, in response to pure tones and down and upward frequency modulated (FM; 50 kHz bandwidth) sweeps. In addition, we calculated current source density (CSD) to test whether lateral intracortical projections facilitate neuronal activation in response to FM echoes containing spectrally distant frequencies from the excitatory frequency response area (FRA). Auditory responses to a set of stimuli changing in frequency and level were recorded along 64 penetrations in the left A1 of six free-tailed bats. FRA shapes were consistent across the cortical depth within a column and there were no obvious differences in tuning properties. Generally, response latencies were shorter (<10 ms) for cortical depths between 500 and 600 µm, which might correspond to thalamocortical input layers IIIb-IV. Most units showed a stronger response to downward FM sweeps, and direction selectivity did not vary across cortical depth. CSD profiles calculated in response to the CF showed a current sink located at depths between 500 and 600 µm. Frequencies lower than the frequency range eliciting a spike response failed to evoke any visible current sink. Frequencies higher than the frequency range producing a spike response evoked layer IV sinks at longer latencies that increased with spectral distance. These data support the hypothesis that a progressive downward relay of spectral information spreads along the tonotopic axis of A1 via lateral connections, contributing to the neural processing of FM down sweeps used in biosonar.

Frequency-modulated up-chirps produce larger evoked responses than down-chirps in the big brown bat auditory brainstem.

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.

Neural timing of stimulus events with microsecond precision.

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.

Echo interval and not echo intensity drives bat flight behavior in structured corridors.

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.

Natural echolocation sequences evoke echo-delay selectivity in the auditory midbrain of the FM bat, Eptesicus fuscus.

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.

Vocal sequences suppress spiking in the bat auditory cortex while evoking concomitant steady-state local field potentials.

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.

Short delays and low pulse amplitudes produce widespread activation in the target-distance processing area of auditory cortex of the mustached bat.

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.

Sharp temporal tuning in the bat auditory midbrain overcomes spectral-temporal trade-off imposed by cochlear mechanics.

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 vocalization sequences broadcasted by bats carry redundant information.

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.

Echo-level compensation and delay tuning in the auditory cortex of the mustached bat.

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.

Temporal encoding precision of bat auditory neurons tuned to target distance deteriorates on the way to the cortex.

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.

Level-tolerant duration selectivity in the auditory cortex of the velvety free-tailed bat Molossus molossus.

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.

Narrow sound pressure level tuning in the auditory cortex of the bats Molossus molossus and Macrotus waterhousii.

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.

Blurry topography for precise target-distance computations in the auditory cortex of echolocating bats.

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.