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.

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 () 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.

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.

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.

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.

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.

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, , 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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Evolution of the heteroharmonic strategy for target-range computation in the echolocation of Mormoopidae.

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.

Neurons in the inferior colliculus of the mustached bat are tuned both to echo-delay and sound duration.

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.

Evolution of neuronal mechanisms for echolocation: specializations for target-range computation in bats of the genus Pteronotus.

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.

Auditory cortex of newborn bats is prewired for echolocation.

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.

Properties of echo delay-tuning receptive fields in the inferior colliculus of the mustached bat.

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.