Long-term changes in cortical representation through perceptual learning of spectrally degraded speech.

Listeners can adapt to acoustically degraded speech with perceptual training. The learning processes for long periods underlies the rehabilitation of patients with hearing aids or cochlear implants. Perceptual learning of acoustically degraded speech has been associated with the frontotemporal cortices. However, neural processes during and after long-term perceptual learning remain unclear. Here we conducted perceptual training of noise-vocoded speech sounds (NVSS), which is spectrally degraded signals, and measured the cortical activity for seven days and the follow up testing (approximately 1 year later) to investigate changes in neural activation patterns using functional magnetic resonance imaging. We demonstrated that young adult participants (n = 5) improved their performance across seven experimental days, and the gains were maintained after 10 months or more. Representational similarity analysis showed that the neural activation patterns of NVSS relative to clear speech in the left posterior superior temporal sulcus (pSTS) were significantly different across seven training days, accompanying neural changes in frontal cortices. In addition, the distinct activation patterns to NVSS in the frontotemporal cortices were also observed 10-13 months after the training. We, therefore, propose that perceptual training can induce plastic changes and long-term effects on neural representations of the trained degraded speech in the frontotemporal cortices. These behavioral improvements and neural changes induced by the perceptual learning of degraded speech will provide insights into cortical mechanisms underlying adaptive processes in difficult listening situations and long-term rehabilitation of auditory disorders.

Neural correlates of subjective comprehension of noise-vocoded speech.

Under an acoustically degraded condition, the degree of speech comprehension fluctuates within individuals. Understanding the relationship between such fluctuations in comprehension and neural responses might reveal perceptual processing for distorted speech. In this study we investigated the cerebral activity associated with the degree of subjective comprehension of noise-vocoded speech sounds (NVSS) using functional magnetic resonance imaging. Our results indicate that higher comprehension of NVSS sentences was associated with greater activation in the right superior temporal cortex, and that activity in the left inferior frontal gyrus (Broca's area) was increased when a listener recognized words in a sentence they did not fully comprehend. In addition, results of laterality analysis demonstrated that recognition of words in an NVSS sentence led to less lateralized responses in the temporal cortex, though a left-lateralization was observed when no words were recognized. The data suggest that variation in comprehension within individuals can be associated with changes in lateralization in the temporal auditory cortex.

Long-latency optical responses from the dorsal inferior colliculus of Seba's fruit bat.

We used a novel microendoscope system to record simultaneously optical activity (fluorescence of a calcium indicator dye) and electrical activity (multi-unit activity and local field potentials) from the dorsal inferior colliculus of the echolocating bat, Carollia perspicillata. Optically recorded calcium responses to wide-band noise and to frequency-modulated bursts were recorded at probe depths down to 1300 µm, with the majority of active sites encountered at more shallow depths down to 800 µm. Calcium activity exhibited long latencies, within the time span of 50-100 ms after stimulus onset, significantly longer than onset latencies of either multi-unit activity or local field potentials. Latencies and amplitude/latency trading of these electrical responses were consistent with those seen in standard electrophysiological recordings, confirming that the microendoscope was able to record both neural and optical activity successfully. Optically recorded calcium responses rose and decayed slowly and were correlated in time with long-latency negative deflections in local field potentials. These data suggest that calcium-evoked responses may reflect known, sustained inhibitory interactions in the inferior colliculus.

Organization of subcortical auditory nuclei of Japanese house bat (Pipistrellus abramus) identified with cytoarchitecture and molecular expression.

The auditory system of echolocating bats shows remarkable specialization likely related to analyzing echoes of sonar pulses. However, significant interspecies differences have been observed in the organization of auditory pathways among echolocating bats, and the homology of auditory nuclei with those of non-echolocating species has not been established. Here, in order to establish the homology and specialization of auditory pathways in echolocating bats, the expression of markers for glutamatergic, GABAergic, and glycinergic phenotypes in the subcortical auditory nuclei of Japanese house bat (Pipistrellus abramus) was evaluated. In the superior olivary complex, we identified the medial superior olive and superior paraolivary nuclei as expressing glutamatergic and GABAergic phenotypes, respectively, suggesting these nuclei are homologous with those of rodents. In the nuclei of the lateral lemniscus (NLL), the dorsal nucleus was found to be purely GABAergic, the intermediate nucleus was a mixture of glutamatergic and inhibitory neurons, the compact part of the ventral nucleus was purely glycinergic, and the multipolar part of the ventral nucleus expressed both GABA and glycine. In the inferior colliculus (IC), the central nucleus was found to be further subdivided into dorsal and ventral parts according to differences in the density of terminals and the morphology of large GABAergic neurons, suggesting specialization to sonar pulse structure. Medial geniculate virtually lacked GABAergic neurons, suggesting that the organization of the tectothalamic pathway is similar with that of rodents. Taken together, our findings revealed that specialization primarily occurs with regard to nuclei size and organization of the NLL and IC.

Acoustic characteristics used by Japanese macaques for individual discrimination.

The vocalizations of primates contain information about speaker individuality. Many primates, including humans, are able to distinguish conspecifics based solely on vocalizations. The purpose of this study was to investigate the acoustic characteristics used by Japanese macaques in individual vocal discrimination. Furthermore, we tested human subjects using monkey vocalizations to evaluate species specificity with respect to such discriminations. Two monkeys and five humans were trained to discriminate the coo calls of two unfamiliar monkeys. We created a stimulus continuum between the vocalizations of the two monkeys as a set of probe stimuli (whole morph). We also created two sets of continua in which only one acoustic parameter, fundamental frequency (f0) or vocal tract characteristic (VTC), was changed from the coo call of one monkey to that of another while the other acoustic feature remained the same (f0 morph and VTC morph, respectively). According to the results, the reaction times both of monkeys and humans were correlated with the morph proportion under the whole morph and f0 morph conditions. The reaction time to the VTC morph was correlated with the morph proportion in both monkeys, whereas the reaction time in humans, on average, was not correlated with morph proportion. Japanese monkeys relied more consistently on VTC than did humans for discriminating monkey vocalizations. Our results support the idea that the auditory system of primates is specialized for processing conspecific vocalizations and suggest that VTC is a significant acoustic feature used by Japanese macaques to discriminate conspecific vocalizations.

Micro-endoscopic system for functional assessment of neural circuits in deep brain regions: Simultaneous optical and electrical recordings of auditory responses in mouse's inferior colliculus.

In vivo Ca2+ imaging is a powerful method for the functional assessment of neural circuits. Although multi-photon excitation fluorescence microscopy has been widely used, observation of circuits in deep brain regions remains challenging. Recently, observing these deep regions has become possible via an endoscope consisting of an optical fiber bundle or gradient-index lens. We have designed a micro-endoscope system that enables simultaneous optical recording of fluorescence and electrical recording of neural activity. Using this system, we recorded auditory responses by simultaneously detecting changes in the fluorescence intensity of a Ca2+ indicator dye, multi-unit activities (MUA), and local field potentials (LFP) in the mouse's inferior colliculus (IC). Such simultaneous optical and electrical recordings enabled detailed comparison of electrically recorded phenomena (MUA and LFP) and optically recorded Ca2+ response. By systematically changing sound frequency and intensity, we determined the frequency tuning of the recording site. The best frequency shifted higher as the probe advanced more deeply, demonstrating that the system is capable of optically measuring the dorso-ventral organization of IC (i.e., tonotopicity). Thus, our new micro-endoscope system will be useful in the neurophysiological studies of a wide range of brain circuits, including those within the auditory system.

Role of vocal tract characteristics in individual discrimination by Japanese macaques (Macaca fuscata).

The Japanese macaque (Macaca fuscata) exhibits a species-specific communication sound called the "coo call" to locate group members and maintain within-group contact. Monkeys have been demonstrated to be capable of discriminating between individuals based only on their voices, but there is still debate regarding how the fundamental frequencies (F0) and filter properties of the vocal tract characteristics (VTC) contribute to individual discrimination in nonhuman primates. This study was performed to investigate the acoustic keys used by Japanese macaques in individual discrimination. Two animals were trained with standard Go/NoGo operant conditioning to distinguish the coo calls of two unfamiliar monkeys. The subjects were required to continue depressing a lever until the stimulus changed from one monkey to the other. The test stimuli were synthesized by combining the F0s and VTC from each individual. Both subjects released the lever when the VTC changed, whereas they did not when the F0 changed. The reaction times to the test stimuli were not significantly different from that to the training stimuli that shared the same VTC. Our data suggest that vocal tract characteristics are important for the identification of individuals by Japanese macaques.

Auditory brainstem responses of Japanese house bats (Pipistrellus abramus) after exposure to broadband ultrasonic noise.

Echolocating bats forage and navigate within an intense soundscape containing their own sonar sounds as well as sounds from other bats. To determine how the bat's auditory system copes with these high noise levels, auditory brainstem responses (ABR) were measured in the Japanese house bat, Pipistrellus abramus, before and after exposure to ultrasonic noise (30 min duration). Noise spectral content (10-80 kHz) and level (90 dB sound pressure level) are within the ranges these bats experience in their natural environment. ABR thresholds to test frequencies of 20, 40, and 80 kHz did not vary significantly between pre-exposure and post-exposure times of 0 and 30 min. Amplitudes and latencies of the P3 wave at suprathreshold were not significantly affected by noise exposure. These data show that the bat's hearing is not compromised when exposed to background sounds similar in wideband frequency content and sound level to what the animal encounters naturally. These results provide a baseline for examining how the bat's auditory system deals with other intense sounds, such as those emitted by anthropogenic sources or those producing temporary threshold shifts in other mammals.

Auditory brainstem response of the Japanese house bat (Pipistrellus abramus).

Auditory brainstem responses (ABR) to high frequencies encompassing the species' vocal repertoire were recorded from the inferior colliculus of the Japanese house bat, Pipistrellus abramus. Amplitudes of tone pips were systematically decreased to obtain a threshold of response at different tone frequencies. The compiled audiogram has a broad U-shape over the frequency range from 4 to 80 kHz, with low thresholds between 20 and 50 kHz. The most sensitive frequency region of 35-50 kHz occurs at the quasi-constant-frequency terminal portion of the bat's downsweeping frequency-modulated echolocation pulses. Good sensitivity extending down to 20 kHz includes the frequency range of the first harmonic of communication sounds. The ABR audiogram does not show distinct, narrow peaks of greater sensitivity at the dominant frequencies in species vocalizations. Latencies of peaks in ABR responses lengthened as stimuli were attenuated. At 40 kHz, response latencies traded with amplitude by -7 to -9 µs/dB, a value smaller than measured in another frequency-modulated bat using lower frequencies for echolocation. These results have implications for understanding the significance of amplitude-latency trading in a comparative context.

Rapid shifts of sonar attention by Pipistrellus abramus during natural hunting for multiple prey.

Flight paths of echolocating Japanese house bats, Pipistrellus abramus, were tracked during insect hunting in a natural setting using a 32-microphone array. The array surrounded the foraging area, locating each bat, and determined the directional aim of the sonar beam. Successive interceptions, indicated by feeding "buzzes" and post-buzz pauses, occurred singly at intervals from over 20 s down to multiple interceptions at 2-3 s intervals. Bats flew on looping, curved paths. Turning radius tightened as rate of interceptions increased, keeping the bat in a smaller area of higher capture density. Broadcast beams shifted direction during search, often alternating between the direction of flight and another direction where, moments later, the next interception would occur. Broadcasts also shifted direction between the current target and the next target. Bats time-share biosonar attention between objects by alternating acoustic gaze. During search, most interpulse intervals (IPIs) were 70-120 ms, but bats interspersed long IPIs up to 200 ms when the rate of interception was low and flight paths followed broad curves. Mathematical modeling of search paths demonstrated that circular flight-paths with occasional long IPIs would be more effective for target search than either random, correlated random, or linear flights.

Adaptive changes in echolocation sounds by Pipistrellus abramus in response to artificial jamming sounds.

The echolocation behavior of Pipistrellus abramus during exposure to artificial jamming sounds during flight was investigated. Echolocation pulses emitted by the bats were recorded using a telemetry microphone mounted on the bats' backs, and their adaptation based on acoustic characteristics of emitted pulses was assessed in terms of jamming-avoidance responses (JARs). In experiment 1, frequency-modulated jamming sounds (3 ms duration) mimicking echolocation pulses of P. abramus were prepared. All bats showed significant increases in the terminal frequency of the frequency-modulated pulse by an average of 2.1-4.5 kHz when the terminal frequency of the jamming sounds was lower than the bats' own pulses. This frequency shift was not observed using jamming frequencies that overlapped with or were higher than the bats' own pulses. These findings suggest that JARs in P. abramus are sensitive to the terminal frequency of jamming pulses and that the bats' response pattern was dependent on the slight difference in stimulus frequency. In experiment 2, when bats were repeatedly exposed to a band-limited noise of 70 ms duration, the bats in flight more frequently emitted pulses during silent periods between jamming sounds, suggesting that the bats could actively change the timing of pulse emissions, even during flight, to avoid temporal overlap with jamming sounds. Our findings demonstrate that bats could adjust their vocalized frequency and emission timing during flight in response to acoustic jamming stimuli.

Prey pursuit strategy of Japanese horseshoe bats during an in-flight target-selection task.

The prey pursuit behavior of Japanese horseshoe bats (Rhinolophus ferrumequinum nippon) was investigated by tasking bats during flight with choosing between two tethered fluttering moths. Echolocation pulses were recorded using a telemetry microphone mounted on the bat combined with a 17-channel horizontal microphone array to measure pulse directions. Flight paths of the bat and moths were monitored using two high-speed video cameras. Acoustical measurements of returning echoes from fluttering moths were first collected using an ultrasonic loudspeaker, turning the head direction of the moth relative to the loudspeaker from 0° (front) to 180° (back) in the horizontal plane. The amount of acoustical glints caused by moth fluttering varied with the sound direction, reaching a maximum at 70°-100° in the horizontal plane. In the flight experiment, moths chosen by the bat fluttered within or moved across these angles relative to the bat's pulse direction, which would cause maximum dynamic changes in the frequency and amplitude of acoustical glints during flight. These results suggest that echoes with acoustical glints containing the strongest frequency and amplitude modulations appear to attract bats for prey selection.

Adaptive beam-width control of echolocation sounds by CF-FM bats, Rhinolophus ferrumequinum nippon, during prey-capture flight.

The echolocation sounds of Japanese CF-FM bats (Rhinolophus ferrumequinum nippon) were measured while the bats pursued a moth (Goniocraspidum pryeri) in a flight chamber. Using a 31-channel microphone array system, we investigated how CF-FM bats adjust pulse direction and beam width according to prey position. During the search and approach phases, the horizontal and vertical beam widths were ±22±5 and ±13±5 deg, respectively. When bats entered the terminal phase approximately 1 m from a moth, distinctive evasive flight by G. pryeri was sometimes observed. Simultaneously, the bats broadened the beam widths of some emissions in both the horizontal (44% of emitted echolocation pulses) and vertical planes (71%). The expanded beam widths were ±36±7 deg (horizontal) and ±30±9 deg (vertical). When moths began evasive flight, the tracking accuracy decreased compared with that during the approach phase. However, in 97% of emissions during the terminal phase, the beam width was wider than the misalignment (the angular difference between the pulse and target directions). These findings indicate that bats actively adjust their beam width to retain the moving target within a spatial echolocation window during the final capture stages.

Audiovisual integration in the primary auditory cortex of an awake rodent.

Much is known about the behavioral and physiological aspects of multimodal integration in primates, whereas less is known about the extent of audiovisual integration in other species. This study investigated the temporal integration of audiovisual stimuli in the primary auditory cortex (A1) of a standard animal model of auditory physiology: the Mongolian gerbil (Meriones unguiculatus). We recorded single unit responses to auditory and visual stimuli in the A1 of awake gerbils. A tone burst (auditory stimulus) paired with a flashing light (visual stimulus) at differing lag times (from 0 to ±160ms) was presented contralateral to the recording site. As a result, the auditory response was altered significantly by the visual stimulus in more than 25% of the A1 units. The effect of the visual stimulus on the auditory response decreased as the time lag between the two modalities increased. The influence of the visual stimulus remained relatively greater when it preceded rather than followed the auditory stimulus. These results suggest that the A1 and earlier (subcortical) auditory structures of the rodent are capable of temporally integrating information from auditory and visual modalities.

Behavioral evidence for auditory induction in a species of rodent: Mongolian gerbil (Meriones unguiculatus).

When a segment of sound of interest is interrupted by a loud extraneous noise, humans perceive that the missing sound continues during the intrusive noise. This restoration of auditory information occurs in perceptions of both speech and non-speech sounds (e.g., tone bursts), a phenomenon referred to as auditory induction. In this study, Mongolian gerbils were trained with standard Go/No-Go operant conditioning to discriminate continuous tone bursts (the Go stimulus) from tone bursts with a silent gap in the middle (the No-Go stimulus). Noise was added to Go and No-Go stimuli to determine the condition under which induction would occur. The Mongolian gerbils engaged in Go responses to No-Go stimuli only when the noise spectrally surrounding the tone was of the same duration as the silent portion of the No-Go stimulus; these results match those previously reported in primates (humans and macaque monkeys). The result presents not only the evidence of the auditory induction in a rodent species but also suggests that similar mechanisms for restoring missing sounds are shared among mammals. Additionally, our findings demonstrated that the rodent can serve as a valuable animal model for future studies of perceptual restoration.

Vocalization of echolocation-like pulses for interindividual interaction in horseshoe bats (Rhinolophus ferrumequinum).

Although much is known about the echolocation of horseshoe bats (Rhinolophus spp.), little is known about the characteristics and function of their communication calls. This study focused on a stereotyped behavior of a bat approaching a companion animal in the colony, and examined their interaction and vocalization during this behavior. The bats emit echolocation-like vocalizations when approaching each other and these vocalizations contain a "buildup" pulse sequence, in which the frequency of the pulse increases gradually to normal echolocation pulse frequencies. The results suggest that the echolocation-like pulses serve an important role in communication within the colony.

Echolocation behavior of the Japanese horseshoe bat in pursuit of fluttering prey.

Echolocation sounds of Rhinolophus ferrumequinum nippon as they approached a fluttering moth (Goniocraspidum pryeri) were investigated using an on-board telemetry microphone (Telemike). In 40% of the successful moth-capture flights, the moth exhibited distinctive evasive flight behavior, but the bat pursued the moth by following its flight path. When the distance to the moth was approximately 3-4 m, the bats increased the duration of the pulses to 65-95 ms, which is 2-3 times longer than those during landing flight (30-40 ms). The mean of 5.8 long pulses were emitted before the final buzz phase of moth capture, without strengthening the sound pressure level. The mean duration of long pulses (79.9 ± 7.9 ms) corresponded to three times the fluttering period of G. pryeri (26.5 × 3 = 79.5 ms). These findings indicate that the bats adjust the pulse duration to increase the number of temporal repetitions of fluttering information rather than to produce more intense sonar sounds to receive fine insect echoes. The bats exhibited Doppler-shift compensation for echoes returning from large static objects ahead, but not for echoes from target moths, even though the bats were focused on capturing the moths. Furthermore, the echoes of the Telemike recordings from target moths showed spectral glints of approximately 1-1.5 kHz caused by the fluttering of the moths but not amplitude glints because of the highly acoustical attenuation of ultrasound in the air, suggesting that spectral information may be more robust than amplitude information in echoes during moth capturing flight.

Convergence of reference frequencies by multiple CF-FM bats (Rhinolophus ferrumequinum nippon) during paired flights evaluated with onboard microphones.

The constant frequency component of the second harmonic (CF(2)) of echolocation sounds in Rhinolophus ferrumequinum nippon were measured using onboard telemetry microphones while the bats exhibited Doppler-shift compensation during flights with conspecifics. (1) The CF(2) frequency of pulses emitted by individual bats at rest (F (rest)) showed a long-term gradual decline by 0.22 kHz on average over a period of 3 months. The mean neighboring F (rest) (interindividual differences in F (rest) between neighboring bats when the bats were arranged in ascending order according to F (rest)) ranged from 0.08 to 0.11 kHz among 18 bats in a laboratory colony. (2) The standard deviation of observed echo CF(2) (reference frequency) for bats during paired flights ranged from 50 to 90 Hz, which was not significantly different from that during single flights. This finding suggests that during paired flights, bats exhibit Doppler-shift compensation with the same accuracy as when they fly alone. (3) In 60% (n = 29) of the cases, the difference in the reference frequency between two bats during paired flights significantly decreased compared to when the bats flew alone. However, only 15% of the cases (n = 7) showed a significant increase during paired flights. The difference in frequency between two bats did not increase even when the reference frequencies of the individuals were not statistically different during single flights.

Classification of vocalizations in the Mongolian gerbil, Meriones unguiculatus.

The Mongolian gerbil (Meriones unguiculatus) has been an important model system in auditory physiology, but its natural sounds are not well known. Vocalizations produced by colonies of adult gerbils were recorded during various social interactions in a standard laboratory animal-rearing facility. Sound recordings were made continuously for 24 h. This species exhibited a rich repertoire of vocalizations that varied in spectrotemporal structure. Calls were classified into 13 distinct syllable types. These syllables were further categorized into eight simple syllables and five composite syllables, which could be described by combinations of two to three simple syllables. The durations of individual syllables ranged from 30 to 330 ms with fundamental frequencies of 5 to 50 kHz. Those with lower fundamental frequencies typically contained more harmonic components (up to nine). Analysis of syllable sequences indicated that syllables may be combined into three types of simple phrases. These results provide a basis for future studies not only of the behavioral significance of vocalization, but also of the neural basis of vocal communication in the Mongolian gerbil.

Developmental changes in ultrasonic vocalizations by infant Japanese echolocating bats, Pipistrellus abramus.

Developmental changes in vocalizations by Pipistrellus abramus were investigated during the first post-natal month. Vocalizations by pups on the day of birth were frequency-modulated ultrasounds from 30.0 ± 4.0 kHz to 19.3 ± 1.9 kHz with multiple harmonics. The terminal frequency of the second harmonic (TF(2)) of pup vocalizations corresponded to that of the fundamental (TF(1)) in adult bats (41.4 ± 2.6 kHz), suggesting that pup vocalizations can be easily detected by the mother. In addition, there are two types of infant vocalization: short duration echolocation precursor and long duration isolation calls, which showed separate developmental patterns over time.