Selective and Efficient Neural Coding of Communication Signals Depends on Early Acoustic and Social Environment

Previous research has shown that postnatal exposure to simple, synthetic sounds can affect the sound representation in the auditory cortex as reflected by changes in the tonotopic map or other relatively simple tuning properties, such as AM tuning. However, their functional implications for neural processing in the generation of ethologically-based perception remain unexplored. Here we examined the effects of noise-rearing and social isolation on the neural processing of communication sounds such as species-specific song, in the primary auditory cortex analog of adult zebra finches. Our electrophysiological recordings reveal that neural tuning to simple frequency-based synthetic sounds is initially established in all the laminae independent of patterned acoustic experience; however, we provide the first evidence that early exposure to patterned sound statistics, such as those found in native sounds, is required for the subsequent emergence of neural selectivity for complex vocalizations and for shaping neural spiking precision in superficial and deep cortical laminae, and for creating efficient neural representations of song and a less redundant ensemble code in all the laminae. Our study also provides the first causal evidence for ‘sparse coding’, such that when the statistics of the stimuli were changed during rearing, as in noise-rearing, that the sparse or optimal representation for species-specific vocalizations disappeared. Taken together, these results imply that a layer-specific differential development of the auditory cortex requires patterned acoustic input, and a specialized and robust sensory representation of complex communication sounds in the auditory cortex requires a rich acoustic and social environment.     

Variation and consistency of female preferences for simulated courtship songs in Drosophila virilis

To study the variation and consistency of song preferences in Drosophila virilis females, we played them species-specific song and songs with modified sound pulses and/or interpulse intervals on 3 consecutive days. Species-specific song was played again on the fourth day. All playbacks were done without the presence of males. About 62% of the females indicated their readiness to mate by spreading their wings in at least one of the trials. The proportion of the females responding to species-specific song was about twice that of the females responding to modified songs. The majority of females responded to only one song type, which suggests that the females varied in their preferences and that their preference windows were rather narrow. The females were consistent in their responsiveness to species-specific song played on 2 days. If the female responded to normal song during the first trial, the probability of her responding to the same song during the second trial increased by about 32%. The number of songs required by the females before responding in the two subsequent trials was also correlated within the females (repeatability 0.328). Repeatability of female preferences for male sexual traits is expected both in the viability and Fisherian models of sexual selection. Copyright 1999 The Association for the Study of Animal Behaviour.     

The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch

The perception of song is vital to the reproductive success of both male and female songbirds. Several neural structures underlying this perception have been identified by examining expression of immediate early genes (IEGs) following the presentation of conspecific or heterospecific song. In the few avian species investigated, areas outside of the circuit for song production contain neurons that are active following song presentation, specifically the caudal hyperstriatum ventrale (cHV) and caudomedial neostriatum (NCM). While studied in detail in the male zebra finch, IEG responses in these neural substrates involved in song perception have not been quantified in females. Therefore, adult female zebra finches were presented with zebra finch song, nonzebra finch song, randomly generated tones, or silence for 30 min. One hour later they were sacrificed, and their brains removed, sectioned, and immunocytochemically processed for FOS expression. Animals exposed to zebra finch song had a significantly higher density of FOS-immunoreactive cells in the NCM than those presented with other songs, tones, or silence. Neuronal activation in the cHV was equivalent in birds that heard zebra finch and non-zebra finch song, expression that was higher than that observed in the groups that heard no song. Interestingly, the hippocampus (HP) and adjacent parahippocampal area (AHP) were activated in a manner comparable to the NCM. These results suggest a general role for the cHV in song perception and a more specific role for the NCM and HP/AHP in facilitating recognition of and responsiveness to species-specific song in female zebra finches.     

Listening to speech in the presence of other sounds

Although most research on the perception of speech has been conducted with speech presented without any competing sounds, we almost always listen to speech against a background of other sounds which we are adept at ignoring. Nevertheless, such additional irrelevant sounds can cause severe problems for speech recognition algorithms and for the hard of hearing as well as posing a challenge to theories of speech perception. A variety of different problems are created by the presence of additional sound sources: detection of features that are partially masked, allocation of detected features to the appropriate sound sources and recognition of sounds on the basis of partial information. The separation of sounds is arousing substantial attention in psychoacoustics and in computer science. An effective solution to the problem of separating sounds would have important practical applications.     

Perception of Vocal Tract Resonances by Whooping Cranes Grus americana

Although formants (vocal tract resonances) can often be observed in avian vocalizations, and several bird species have been shown to perceive formants in human speech sounds, no studies have examined formant perception in birds' own species-specific calls. We used playbacks of computer-synthesized crane calls in a modified habituation—dishabituation paradigm to test for formant perception in whooping cranes ( Grus americana ). After habituating birds to recordings of natural contact calls, we played a synthesized replica of one of the habituating stimuli as a control to ensure that the synthesizer worked adequately; birds dishabituated in only one of 13 cases. Then, we played the same call with its formant frequencies shifted. The birds dishabituated to the formant-shifted calls in 10 out of 12 playbacks. These data suggest that cranes perceive and attend to changes in formant frequencies in their own species-specific vocalizations, and are consistent with the hypothesis that formants can provide acoustic cues to individuality and body size.     

Social Behaviour on the Wing in the False Vampire,Megaderma lyra

Social interaction occurs in bats. In a group of 10 Megaderma lyra (seven female and two male adults, as well as one female juvenile) held in captivity, two stereotyped flying behaviour patterns —the ‘grumbling flight’ and the ‘song flight’ — were observed and studied. The ‘grumbling flight’ is a social interaction in flight between at least two Megaderma lyra in which ‘grumble sequences’ are emitted. This behaviour is triggered by stress or arising aggression, and presumably attempts to avoid agonistic interactions with dangerous physical contact. The song flight was exclusively displayed by the dominant male bat and only directed at the non-lactating female members of the group, with a preference to alien females. This behaviour is composed of three behavioural stages, each accompanied by a specific ‘song strophe’. The song flight presumably aims at bonding the females to the male. During the grumbling flight and the song flight, M. lyra emits communication sounds in the ultrasonic range. The sounds consist of simple elements (FM_down, FM_up, CF), and are similar to types of sounds emitted for echolocation by various bat species.     

Spatial perception of stimuli during unilateral exclusion of the temporal portion of the neocortex by cold]

Behavioral reaction of twelve cats were studied in conditions of inactivation by cold of the temporal area (AI, AII, Ep and partly I-T) of one hemisphere. A typical vestibular ataxy was observed: deflection of the cats when walking, circular movements in the direction of the inactivated temporal area. Orienting reactions both to acoustic and photic stimuli persisted, but their spatial localization was completely lost. In every case the animals exhibited a clear orienting reaction towards the inactivated hemisphere, regardless of the localization of the source of signal. Reactions ot pain and olfactory stimulations likewise proceded in one direction. such a one-sided perception of sounds in the case of inactivation by cold of the temporal neocortex of one hemispheres is apparently due to the functional elimination of contralateral auditory structures. Disturbance of adequate spatial perception of photic, pain and olfactory stimuli under similar conditions results from a sharp drop in the tone predominantly of the ipsilateral hemisphere.     

Grouping in auditory temporal perception and vocal production is mutually adapted: the case of wriggling calls of mice

Auditory Gestalt perception by grouping of species-specific vocalizations to a perceptual stream with a defined meaning is typical for human speech perception but has not been studied in non-human mammals so far. Here we use synthesized models of vocalizations (series of wriggling calls) of mouse pups (Mus domesticus) and show that their mothers perceive the call series as a meaningful Gestalt for the release of instinctive maternal behavior, if the inter-call intervals have durations of 100–400 ms. Shorter or longer inter-call intervals significantly reduce the maternal responsiveness. We also show that series of natural wriggling calls have inter-call intervals mainly in the range of 100–400 ms. Thus, series of natural wriggling calls of pups match the time-domain auditory filters of their mothers in order to be optimally perceived and recognized. A similar time window exists for the production of human speech and the perception of series of sounds by humans. Neural mechanisms for setting the boundaries of the time window are discussed.     

Phonological representations are unconsciously used when processing complex, non-speech signals

Neuroimaging studies of speech processing increasingly rely on artificial speech-like sounds whose perceptual status as speech or non-speech is assigned by simple subjective judgments; brain activation patterns are interpreted according to these status assignments. The naïve perceptual status of one such stimulus, spectrally-rotated speech (not consciously perceived as speech by naïve subjects), was evaluated in discrimination and forced identification experiments. Discrimination of variation in spectrally-rotated syllables in one group of naïve subjects was strongly related to the pattern of similarities in phonological identification of the same stimuli provided by a second, independent group of naïve subjects, suggesting either that (1) naïve rotated syllable perception involves phonetic-like processing, or (2) that perception is solely based on physical acoustic similarity, and similar sounds are provided with similar phonetic identities. Analysis of acoustic (Euclidean distances of center frequency values of formants) and phonetic similarities in the perception of the vowel portions of the rotated syllables revealed that discrimination was significantly and independently influenced by both acoustic and phonological information. We conclude that simple subjective assessments of artificial speech-like sounds can be misleading, as perception of such sounds may initially and unconsciously utilize speech-like, phonological processing.     

Neurophysiological response selectivity for conspecific songs over synthetic sounds in the auditory forebrain of non-singing female songbirds

Female choice plays a critical role in the evolution of male acoustic displays. Yet there is limited information on the neurophysiological basis of female songbirds’ auditory recognition systems. To understand the neural mechanisms of how non-singing female songbirds perceive behaviorally relevant vocalizations, we recorded responses of single neurons to acoustic stimuli in two auditory forebrain regions, the caudal lateral mesopallium (CLM) and Field L, in anesthetized adult female zebra finches (Taeniopygia guttata). Using various metrics of response selectivity, we found consistently higher response strengths for unfamiliar conspecific songs compared to tone pips and white noise in Field L but not in CLM. We also found that neurons in the left auditory forebrain had lower response strengths to synthetics sounds, leading to overall higher neural selectivity for song in neurons of the left hemisphere. This laterality effect is consistent with previously published behavioral data in zebra finches. Overall, our results from Field L are in parallel and from CLM are in contrast with the patterns of response selectivity reported for conspecific songs over synthetic sounds in male zebra finches, suggesting some degree of sexual dimorphism of auditory perception mechanisms in songbirds.     

Behavioral and neural lateralization of vision in courtship singing of the zebra finch

Along with human speech and language processing, birdsong has been one of the best-characterized model systems for understanding the relationship of lateralization of brain function to behavior. Lateralization of song production has been extensively characterized, and lateralization of song perception has begun to be studied. Here we have begun to examine whether behavior and brain function are lateralized in relation to communicative aspects of singing, as well. In order to monitor central brain function, we assayed the levels of several activity dependent immediate early genes after directed courtship singing. Consistent with a lateralization of visual processing during communication, there were higher levels of expression of both egr-1 and c-fos in the left optic tectum after directed singing. Because input from the eyes to the brain is almost completely contralateral in birds, these results suggest that visual input from the right eye should be favored during normal singing to females. Consistent with this, we further found that males sang more when they could use only their right eye compared to when they could use only their left eye. Normal levels of singing, though, required free use of both eyes to view the female. These results suggest that there is a preference for visual processing by the right eye and left brain hemisphere during courtship singing. This may reflect a proposed specialization of the avian left hemisphere in sustaining attention on stimuli toward which a motor response is planned.     

Coding of communication calls in the subcortical and cortical structures of the auditory system

The processing of species-specific communication signals in the auditory system represents an important aspect of animal behavior and is crucial for its social interactions, reproduction, and survival. In this article the neuronal mechanisms underlying the processing of communication signals in the higher centers of the auditory system--inferior colliculus (IC), medial geniculate body (MGB) and auditory cortex (AC)--are reviewed, with particular attention to the guinea pig. The selectivity of neuronal responses for individual calls in these auditory centers in the guinea pig is usually low--most neurons respond to calls as well as to artificial sounds; the coding of complex sounds in the central auditory nuclei is apparently based on the representation of temporal and spectral features of acoustical stimuli in neural networks. Neuronal response patterns in the IC reliably match the sound envelope for calls characterized by one or more short impulses, but do not exactly fit the envelope for long calls. Also, the main spectral peaks are represented by neuronal firing rates in the IC. In comparison to the IC, response patterns in the MGB and AC demonstrate a less precise representation of the sound envelope, especially in the case of longer calls. The spectral representation is worse in the case of low-frequency calls, but not in the case of broad-band calls. The emotional content of the call may influence neuronal responses in the auditory pathway, which can be demonstrated by stimulation with time-reversed calls or by measurements performed under different levels of anesthesia. The investigation of the principles of the neural coding of species-specific vocalizations offers some keys for understanding the neural mechanisms underlying human speech perception.     

Song discrimination by nestling collared flycatchers during early development

Pre-zygotic isolation is often maintained by species-specific signals and preferences. However, in species where signals are learnt, as in songbirds, learning errors can lead to costly hybridization. Song discrimination expressed during early developmental stages may ensure selective learning later in life but can be difficult to demonstrate before behavioural responses are obvious. Here, we use a novel method, measuring changes in metabolic rate, to detect song perception and discrimination in collared flycatcher embryos and nestlings. We found that nestlings as early as 7 days old respond to song with increased metabolic rate, and, by 9 days old, have increased metabolic rate when listening to conspecific when compared with heterospecific song. This early discrimination between songs probably leads to fewer heterospecific matings, and thus higher fitness of collared flycatchers living in sympatry with closely related species.     

长颚斗蟋的鸣声结构与行为分析

通过计算机外接话筒对长颚斗蟋（Velarifictorus asperses)在不同条件下的鸣声进行录音,利用软作Cool edit2000对其结构进行了较系统的分析。结果表明：长颚斗蟋的鸣叫声有7种类型,即召唤声,警戒声,挑衅声,胜利声,欢迎声,求爱声和催促声;这7种鸣声在声学特征上有明显的区别,并与行为有关。     

How social experience shapes song representation in the brain of starlings

Birdsong, like speech, is a learned behaviour whose critical function is to communicate with others and whose development critically depends on social influences. Song learning is a complex phenomenon that involves not only the development of species-specific vocalisations, but also the development of the ability to organise these vocalisations and to use them in an appropriate context. Although the fact that interactions with adult experienced models are essential for song production to develop properly has been well established, far less is known about song perception and processing. The fact that songbirds learn to vocalise and to use their vocalisations selectively through interactions with adults questions whether such interactions are also required for songbirds to perceive and process their vocalisations selectively and whether social interactions may shape song perception and processing as they shape song production. In order to address these questions, our team uses an original neuroethological approach to study the neural bases of song behaviour in a highly social songbird species: the European starlings. We provide here a synthesis of the results we have obtained using this approach over the last decade. Our results show that direct social experience with adult experienced models not only shapes song behaviour but also shapes these songbirds’ brains and their ability to perceive and to process acoustic signals whose communicative value, as well as their acoustic structure, have to be learned.     

Courtship-sounds and behaviour in the four species of the Drosophila bipectinata complex

The D. bipectinata complex contains four species which are sympatric over parts of their range. They are morphologically identical and hybridize in no-choice mating situations. They have similar but distinct courtship patterns and males of all species sing two songs, long song early and short song late in courtship. Each species has a unique song profile due to differences in at least one song parameter. This is circumstantial evidence that sounds function to maintain sexual isolation within the complex.     

The interplay of within-species perceptual predispositions and experience during song ontogeny in zebra finches (Taeniopygia guttata)

Vocal acquisition in songbirds and humans shows many similarities, one of which is that both involve a combination of experience and perceptual predispositions. Among languages some speech sounds are shared, while others are not. This could reflect a predisposition in young infants for learning some speech sounds over others, which combines with exposure-based learning. Similarly, in songbirds, some sounds are common across populations, while others are more specific to populations or individuals. We examine whether this is also due to perceptual preferences for certain within-species element types in naive juvenile male birds, and how such preferences interact with exposure to guide subsequent song learning. We show that young zebra finches lacking previous song exposure perceptually prefer songs with more common zebra finch song element types over songs with less common elements. Next, we demonstrate that after subsequent tutoring, birds prefer tutor songs regardless of whether these contain more common or less common elements. In adulthood, birds tutored with more common elements showed a higher song similarity to their tutor song, indicating that the early bias influenced song learning. Our findings help to understand the maintenance of similarities and the presence of differences among birds'' songs, their dialects and human languages.     

A potential neural substrate for processing functional classes of complex acoustic signals

Categorization is essential to all cognitive processes, but identifying the neural substrates underlying categorization processes is a real challenge. Among animals that have been shown to be able of categorization, songbirds are particularly interesting because they provide researchers with clear examples of categories of acoustic signals allowing different levels of recognition, and they possess a system of specialized brain structures found only in birds that learn to sing: the song system. Moreover, an avian brain nucleus that is analogous to the mammalian secondary auditory cortex (the caudo-medial nidopallium, or NCM) has recently emerged as a plausible site for sensory representation of birdsong, and appears as a well positioned brain region for categorization of songs. Hence, we tested responses in this non-primary, associative area to clear and distinct classes of songs with different functions and social values, and for a possible correspondence between these responses and the functional aspects of songs, in a highly social songbird species: the European starling. Our results clearly show differential neuronal responses to the ethologically defined classes of songs, both in the number of neurons responding, and in the response magnitude of these neurons. Most importantly, these differential responses corresponded to the functional classes of songs, with increasing activation from non-specific to species-specific and from species-specific to individual-specific sounds. These data therefore suggest a potential neural substrate for sorting natural communication signals into categories, and for individual vocal recognition of same-species members. Given the many parallels that exist between birdsong and speech, these results may contribute to a better understanding of the neural bases of speech.     

Sounds recorded in salt marshes and attributed to the European eel

The sounds were recorded in coastal ponds off the French Atlantic coast. They are characterized by continuous series of regularly spaced sounds, each sound being composed of one to four pulses of 7.8-ms duration. The main frequencies of these sounds are under 350 Hz. Due to the special characteristics of these sounds, their temporal patterning, their coastal pond provenance and their close similarity to sounds made by the American eel (Anguilla rostrata), we attribute them to the European eel (Anguilla anguilla).