Kohta I. Kobayasi

A Mechanism for Vocal-Respiratory Coupling in the Mammalian Parabrachial Nucleus

Mammalian vocalizations require the precise coordination of separate laryngeal and respiratory motor pathways. Precisely how and where in the brain vocal motor patterns interact with respiratory rhythm control is unknown. The parabrachial nucleus (PB) is known to mediate key respiratory reflexes and is also considered a principle component of the mammalian vocal motor pathway, making it a likely site for vocal-respiratory interactions, yet a specific role for the PB in vocalizing has yet to be demonstrated. To investigate the role of the PB in vocal-respiratory coordination, we pharmacologically manipulated synaptic activity in the PB while spontaneously vocalizing horseshoe bats were provoked to emit either short, single syllable or long, multisyllabic vocal motor patterns. Iontophoresis of the GABAA agonist muscimol (MUS) into the lateral PB extended expiratory durations surrounding all vocalizations and increased mean call durations. Alternatively, application of the GABAA antagonist bicuculline methiodide (BIC) shortened expirations and call durations. In addition, BIC eliminated the occurrence of multisyllabic vocalizations. BIC caused a mild increase in quiet breathing rates, whereas MUS tended to slow quiet breathing. The results indicate that GABAA receptor-mediated inhibition in the lateral PB modulates the time course of respiratory phase switching during vocalizing, and is needed for proper coordination of calling and breathing in mammals. We hypothesize that vocal-respiratory rhythm entrainment is achieved at least in part via mechanisms similar to other forms of locomotor-respiratory coupling, namely somatosensory feedback influences on respiratory phase-switching in the lateral PB.

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.

Behavioural and neurobiological implications of linear and non-linear features in larynx phonations of horseshoe bats

Mammalian vocalizations exhibit large variations in their spectrotemporal features, although it is still largely unknown which result from intrinsic biomechanical properties of the larynx and which are under direct neuromuscular control. Here we show that mere changes in laryngeal air flow yield several non-linear effects on sound production, in an isolated larynx preparation from horseshoe bats. Most notably, there are sudden jumps between two frequency bands used for either echolocation or communication in natural vocalizations. These jumps resemble changes in “registers” as in yodelling. In contrast, simulated contractions of the main larynx muscle produce linear frequency changes, but are limited to echolocation or communication frequencies. Only by combining non-linear and linear properties can this larynx therefore produce sounds covering the entire frequency range of natural calls. This may give behavioural meaning to yodelling-like vocal behaviour and reshape our thinking about how the brain controls the multitude of spectral vocal features in mammals.

Sex differences in amplitude regulation of distance calls in Bengalese finches, Lunchula striata var. domestica

Many animals regulate their vocal amplitude in relation to environmental noise levels. This behaviour is important both for maintaining auditory feedback and for long distance communication. In this experiment we asked two specific questions. Firstly, does the Bengalese finch, a species of songbirds that critically relies on immediate auditory feedback for its vocalisations, change the amplitude of distance calls against noise? Secondly, if it does, is there any difference between the sexes in the degree of amplitude regulation? To answer these, we recorded distance calls of male and female Bengalese finches under various noise conditions and compared amplitude regulation between the sexes. Results suggest that the finches do show amplitude regulation and that the degree of compensation is much stronger in males than in females. Results are discussed in view of the sex differences in neural mechanisms and the function of distance calls in this species.

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 control in Mongolian gerbils (Meriones unguiculatus) during locomotion behavior

The vocalization behavior of Mongolian gerbils, a model animal of auditory physiology, was examined. A pair of gerbils was placed in a chamber, and their species-specific vocalizations and locomotive behaviors were recorded and analyzed. Two types of calls were predominantly produced: high-frequency upward frequency-modulated (HU-FM) calls and low-frequency multi-harmonic frequency-modulated (LM-FM) calls. Emission rates of HU-FM calls significantly decreased as the distance between the two gerbils increased, and playback of simulated HU-FM calls increased the emission rates. Acoustic analysis of HU-FM calls showed that the calls exhibited a stereotypic spectro-temporal structure including a fixed inter-onset interval (100-175 ms) and that individual differences in the frequency could convey the body size of the callers. The timing of HU-FM calls was highly synchronized with jump movements when an animal vocalized while jumping, suggesting the existence of tight locomotor-vocal coupling. Conversely, LM-FM calls were observed only when the gerbils tactilely contacted with each other while fighting over a food. These results suggest that Mongolian gerbils change the rates of call emissions and call types (e.g., LM-FM or HU-FM calls) in response to changes in visual and possibly tactile and auditory information. The functions of both calls are discussed in terms of their acoustic structures.

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.

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.

Rapid frequency control of sonar sounds by the FM bat, Miniopterus fuliginosus, in response to spectral overlap

In the presence of multiple flying conspecifics, echolocating bats avoid jamming by adjusting the spectral and/or temporal features of their vocalizations. However, little is known about how bats alter their pulse acoustic characteristics to adapt to an acoustically jamming situation during flight. We investigated echolocation behavior in a bat (Miniopterus fuliginosus) during free flight under acoustic jamming conditions created by downward FM jamming sounds mimicking bat echolocation sounds. In an experimental chamber, the flying bat was exposed to FM jamming sounds with different terminal frequencies (TFs) from loudspeakers. Echolocation pulses emitted by the flying bat were recorded using a telemetry microphone (Telemike) mounted on the back of the bat. The bats immediately (within 150ms) shifted the TFs of emitted pulses upward when FM jamming sounds were presented. Moreover, the amount of upward TF shift differed depending on the TF ranges of the jamming sounds presented. When the TF range was lower than or overlapped the bats mean TF, the bat TF shifted significantly upward (by 1-2kHz, Students t-test, P<0.05), corresponding to 3-5% of the total bandwidth of their emitted pulses. These findings indicate that bats actively avoid overlap of the narrow frequency band around the TF.

Bats enhance their call identities to solve the cocktail party problem

Echolocating bats need to solve the problem of signal jamming by conspecifics when they are in a group. However, while several mechanisms have been suggested, it remains unclear how bats avoid confusion between their own echoes and interfering sounds in a complex acoustic environment. Here, we fixed on-board microphones onto individual frequency-modulating bats flying in groups. We found that group members broaden the inter-individual differences in the terminal frequencies of pulses, thereby decreasing the similarity of pulses among individuals. To understand what features most affect similarity between pulses, we calculated the similarity of signals mimicking pulses. We found that the similarity between those artificial signals was decreased most by manipulation of terminal frequency. These results demonstrate that the signal jamming problem is solved by this simple strategy, which may be universally used by animals that use active sensing, such as echolocating bats and electric fish, thereby transcending species and sensory modalities.Kazuma Hase et al. use microphones mounted directly on bats flying in groups to understand how they avoid confusing the echolocation signals of multiple individuals. They find that bats manipulate the terminal frequencies of their signal pulses to decrease the similarity in pulses between individuals.