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

George I, Cousillas H, Richard JP, Hausberger M - PLoS ONE (2008)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Université Rennes 1, CNRS, UMR 6552 Ethologie Animale et Humaine, Rennes, France. isabelle.george@univ-rennes1.fr

ABSTRACT
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.

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Stimuli used to test the neurons, with some examples of sonograms.Class-I songs are whistles that are produced by all male starlings and that are used in species and population recognition, as confirmed by playback experiments with dialectal variants [29], [30]. Among these songs, 4 themes can be distinguished (from left to right and from top to bottom): harmonic themes (HT), inflection themes (IT), rhythmic themes (RT), and simple themes (ST). Two unfamiliar variants of each theme were used. Class-II songs are individual-specific whistles that are used in long-distance recognition, and that can be shared, in captivity, by a few socially affiliated birds [31]. Two exemplars from the tested bird (own), 2 unfamiliar and 2 familiar exemplars were used. A familiar exemplar was a song produced by a bird that had been caught at the same time as the tested bird, and that had spent 2 years in the same aviary. Class-III songs, also called warbling, are mainly composed of highly individual motifs but also of some motifs common to all starlings [32], [33]. They are used in short distance communication. One species-specific motif (clicks) and two individual-specific motifs (one unfamiliar and one from the tested bird) were used. Finally, 5 pure tones (0.5, 1 , 2, 4 and 8 kHz) and a white noise were used as artificial non-specific stimuli. The stimuli (n = 23) were the same for all the birds except those corresponding to the bird's own songs and to the familiar songs, which changed from one bird to another.
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pone-0002203-g001: Stimuli used to test the neurons, with some examples of sonograms.Class-I songs are whistles that are produced by all male starlings and that are used in species and population recognition, as confirmed by playback experiments with dialectal variants [29], [30]. Among these songs, 4 themes can be distinguished (from left to right and from top to bottom): harmonic themes (HT), inflection themes (IT), rhythmic themes (RT), and simple themes (ST). Two unfamiliar variants of each theme were used. Class-II songs are individual-specific whistles that are used in long-distance recognition, and that can be shared, in captivity, by a few socially affiliated birds [31]. Two exemplars from the tested bird (own), 2 unfamiliar and 2 familiar exemplars were used. A familiar exemplar was a song produced by a bird that had been caught at the same time as the tested bird, and that had spent 2 years in the same aviary. Class-III songs, also called warbling, are mainly composed of highly individual motifs but also of some motifs common to all starlings [32], [33]. They are used in short distance communication. One species-specific motif (clicks) and two individual-specific motifs (one unfamiliar and one from the tested bird) were used. Finally, 5 pure tones (0.5, 1 , 2, 4 and 8 kHz) and a white noise were used as artificial non-specific stimuli. The stimuli (n = 23) were the same for all the birds except those corresponding to the bird's own songs and to the familiar songs, which changed from one bird to another.

Mentions: Previous studies thus point to NCM as a well positioned brain region for categorization of songs with different functions and social values. For this reason, we hypothesized that, in our model songbird, which is the starling, NCM neurons may respond differentially to the distinct functional classes of songs that have been described in this highly social species. Indeed, male starlings sing three structurally and functionally distinct classes of songs that are used for species, population and individual recognition (see Fig. 1 for examples) [28]. Class-I songs are short, simple and loud whistles sung by all male starlings that are used in species and population recognition (dialectal variants) [29], [30]. Class-II songs are also short, simple and loud whistles that are used in individual recognition, especially between same-sex social partners [31]. Finally, class-III songs, also called warbling, are long, complex and soft songs that are used in individual recognition at short distance, especially between males and females [32], [33]. These three classes of songs differ not only by their structure [34], [35], but also by their pattern of acquisition during song learning [36]–[38], and by their context of emission [29], [39]–[42]. They thus correspond to clear and distinct classes of sounds with different functions and social values. Hence, we used these songs to test for potential differential responses in the NCM of awake-restrained adult male starlings and for a possible correspondence between these responses and the functional aspects of songs. Our study demonstrates that the activity of NCM neurons can indeed indicate or represent a class of sounds corresponding to a behaviourally-defined recognition process.


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

George I, Cousillas H, Richard JP, Hausberger M - PLoS ONE (2008)

Stimuli used to test the neurons, with some examples of sonograms.Class-I songs are whistles that are produced by all male starlings and that are used in species and population recognition, as confirmed by playback experiments with dialectal variants [29], [30]. Among these songs, 4 themes can be distinguished (from left to right and from top to bottom): harmonic themes (HT), inflection themes (IT), rhythmic themes (RT), and simple themes (ST). Two unfamiliar variants of each theme were used. Class-II songs are individual-specific whistles that are used in long-distance recognition, and that can be shared, in captivity, by a few socially affiliated birds [31]. Two exemplars from the tested bird (own), 2 unfamiliar and 2 familiar exemplars were used. A familiar exemplar was a song produced by a bird that had been caught at the same time as the tested bird, and that had spent 2 years in the same aviary. Class-III songs, also called warbling, are mainly composed of highly individual motifs but also of some motifs common to all starlings [32], [33]. They are used in short distance communication. One species-specific motif (clicks) and two individual-specific motifs (one unfamiliar and one from the tested bird) were used. Finally, 5 pure tones (0.5, 1 , 2, 4 and 8 kHz) and a white noise were used as artificial non-specific stimuli. The stimuli (n = 23) were the same for all the birds except those corresponding to the bird's own songs and to the familiar songs, which changed from one bird to another.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2376065&req=5

pone-0002203-g001: Stimuli used to test the neurons, with some examples of sonograms.Class-I songs are whistles that are produced by all male starlings and that are used in species and population recognition, as confirmed by playback experiments with dialectal variants [29], [30]. Among these songs, 4 themes can be distinguished (from left to right and from top to bottom): harmonic themes (HT), inflection themes (IT), rhythmic themes (RT), and simple themes (ST). Two unfamiliar variants of each theme were used. Class-II songs are individual-specific whistles that are used in long-distance recognition, and that can be shared, in captivity, by a few socially affiliated birds [31]. Two exemplars from the tested bird (own), 2 unfamiliar and 2 familiar exemplars were used. A familiar exemplar was a song produced by a bird that had been caught at the same time as the tested bird, and that had spent 2 years in the same aviary. Class-III songs, also called warbling, are mainly composed of highly individual motifs but also of some motifs common to all starlings [32], [33]. They are used in short distance communication. One species-specific motif (clicks) and two individual-specific motifs (one unfamiliar and one from the tested bird) were used. Finally, 5 pure tones (0.5, 1 , 2, 4 and 8 kHz) and a white noise were used as artificial non-specific stimuli. The stimuli (n = 23) were the same for all the birds except those corresponding to the bird's own songs and to the familiar songs, which changed from one bird to another.
Mentions: Previous studies thus point to NCM as a well positioned brain region for categorization of songs with different functions and social values. For this reason, we hypothesized that, in our model songbird, which is the starling, NCM neurons may respond differentially to the distinct functional classes of songs that have been described in this highly social species. Indeed, male starlings sing three structurally and functionally distinct classes of songs that are used for species, population and individual recognition (see Fig. 1 for examples) [28]. Class-I songs are short, simple and loud whistles sung by all male starlings that are used in species and population recognition (dialectal variants) [29], [30]. Class-II songs are also short, simple and loud whistles that are used in individual recognition, especially between same-sex social partners [31]. Finally, class-III songs, also called warbling, are long, complex and soft songs that are used in individual recognition at short distance, especially between males and females [32], [33]. These three classes of songs differ not only by their structure [34], [35], but also by their pattern of acquisition during song learning [36]–[38], and by their context of emission [29], [39]–[42]. They thus correspond to clear and distinct classes of sounds with different functions and social values. Hence, we used these songs to test for potential differential responses in the NCM of awake-restrained adult male starlings and for a possible correspondence between these responses and the functional aspects of songs. Our study demonstrates that the activity of NCM neurons can indeed indicate or represent a class of sounds corresponding to a behaviourally-defined recognition process.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Université Rennes 1, CNRS, UMR 6552 Ethologie Animale et Humaine, Rennes, France. isabelle.george@univ-rennes1.fr

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus