A quantitative method for analyzing species-specific vocal sequence pattern and its developmental dynamics

Imai, Raimu; Sawai, Azusa; Hayase, Shin; Furukawa, Hiroyuki; Asogwa, Chinweike Norman; Sánchez, Miguel; Wang, Hongdi; Mori, Chihiro; Wada, Kazuhiro

doi:10.1016/j.jneumeth.2016.06.023

Cited by 13 publications

(27 citation statements)

References 32 publications

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“…We found a statistically significant difference in chrm2 expression levels among the six species ( Figure b, Kruskal–Wallis test, *** p < .0001). Although these songbird species exhibit species‐unique vocal patterns (Figure a) (Imai et al, ), we could not detect an apparent link between song phenotypes, particularly the syllable sequence and chrm2 expression in HVC. For example, although both CN and OF produce repetitive sequence‐based song patterns, chrm2 expression in HVC was high in OF but suppressed in CN.…”

Section: Resultscontrasting

confidence: 62%

Inter‐ and intra‐specific differences in muscarinic acetylcholine receptor expression in the neural pathways for vocal learning in songbirds

Asogwa

Mori

Sánchez-Valpuesta

et al. 2018

J of Comparative Neurology

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Acetylcholine receptors (AChRs) abound in the central nervous system of vertebrates. Muscarinic AChRs (mAChRs), a functional subclass of AChRs, mediate neuronal responses via intracellular signal transduction. They also play roles in sensorimotor coordination and motor skill learning by enhancing cortical plasticity. Learned birdsong is a complex motor skill acquired through sensorimotor coordination during a critical period. However, the functions of AChRs in the neural circuits for vocal learning and production remain largely unexplored. Here, we report the unique expression of mAChRs subunits (chrm2-5) in the song nuclei of zebra finches. The expression of excitatory subunits (chrm3 and chrm5) was downregulated in the song nuclei compared with the surrounding brain regions. In contrast, the expression of inhibitory mAChRs (chrm2 and chrm4) was upregulated in the premotor song nucleus HVC relative to the surrounding nidopallium. Chrm4 showed developmentally different expression in HVC during the critical period. Compared with chrm4, individual differences in chrm2 expression emerged in HVC early in the critical period. These individual differences in chrm2 expression persisted despite testosterone administration or auditory deprivation, which altered the timing of song stabilization. Instead, the variability in chrm2 expression in HVC correlated with parental genetics. In addition, chrm2 expression in HVC exhibited species differences and individual variability among songbird species. These results suggest that mAChRs play an underappreciated role in the development of species and individual differences in song patterns by modulating the excitability of HVC neurons, providing a potential insight into the gating of auditory responses in HVC neurons.

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Section: Resultscontrasting

confidence: 62%

Inter‐ and intra‐specific differences in muscarinic acetylcholine receptor expression in the neural pathways for vocal learning in songbirds

Asogwa

Mori

Sánchez-Valpuesta

et al. 2018

J of Comparative Neurology

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“…First, we compared the song features of ZF and OF reared with conspecific song tutoring in our breeding colony to confirm whether a laboratory-controlled environment could maintain species-specific song features. We compared the songs of the two species regarding syllable acoustics and sequential features (12 parameters) at the adult stage ( Fig 2A ) and identified significant differences in six acoustic syllable parameters (i.e., syllable duration, inter-syllable gap duration, entropy variance, amplitude modulation [AM] variance, mean frequency modulation [FM], and FM variance) and in syllable sequence features (motif and repetition transition rates) ( n = 6 birds each, p < 0.01, one-way ANOVA) ( Fig 2B and 2C and S1 Fig ) [30, 31]. We found that the range but not the pattern of each acoustic feature’s distribution overlapped between ZFs and OFs (3,000 syllables from n = 6 birds each and 500 syllables/bird) ( S1 Fig ), thus suggesting that the species differences in the syllable acoustics were not caused by physical species-specific constraints in the peripheral vocal organs.…”

Section: Resultsmentioning

confidence: 99%

“…Statistical analysis was performed on these acoustic features between ZF and OF by one-way ANOVA. For the analysis of the sequence feature of songs (motif and repetition rates in a song), a syllable similarity matrix (SSM) analysis was performed following a previously reported method [30] ( S1 Fig ). This method calculates the contiguous syllables transition frequency of “paired (motif)” and “repetitive” syllables transitions in the songs.…”

Section: Methodsmentioning

confidence: 99%

Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds

et al. 2019

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Learning of most motor skills is constrained in a species-specific manner. However, the proximate mechanisms underlying species-specific learned behaviors remain poorly understood. Songbirds acquire species-specific songs through learning, which is hypothesized to depend on species-specific patterns of gene expression in functionally specialized brain regions for vocal learning and production, called song nuclei. Here, we leveraged two closely related songbird species, zebra finch, owl finch, and their interspecific first-generation (F1) hybrids, to relate transcriptional regulatory divergence between species with the production of species-specific songs. We quantified genome-wide gene expression in both species and compared this with allele-specific expression in F1 hybrids to identify genes whose expression in song nuclei is regulated by species divergence in either cis- or trans-regulation. We found that divergence in transcriptional regulation altered the expression of approximately 10% of total transcribed genes and was linked to differential gene expression between the two species. Furthermore, trans-regulatory changes were more prevalent than cis-regulatory and were associated with synaptic formation and transmission in song nucleus RA, the avian analog of the mammalian laryngeal motor cortex. We identified brain-derived neurotrophic factor (BDNF) as an upstream mediator of trans-regulated genes in RA, with a significant correlation between individual variation in BDNF expression level and species-specific song phenotypes in F1 hybrids. This was supported by the fact that the pharmacological overactivation of BDNF receptors altered the expression of its trans-regulated genes in the RA, thus disrupting the learned song structures of adult zebra finch songs at the acoustic and sequence levels. These results demonstrate functional neurogenetic associations between divergence in region-specific transcriptional regulation and species-specific learned behaviors.

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“…Introductory notes in a song were not included for analyses. The series of separated syllable files of songs were transferred to the CORRELATOR program of Avisoft SASLab pro (Avisoft Bioacoustics, Berlin, Germany) for calculating the similarity scores between the syllables from pupils’ and tutors’ songs by the round-robin comparison [ 73 ]. The highest similarity score for each syllable of pupil songs against tutor syllables was averaged as the similarity score of total syllables for each individual.…”

Section: Methodsmentioning

confidence: 99%

Vocal practice regulates singing activity–dependent genes underlying age-independent vocal learning in songbirds

et al. 2018

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The development of highly complex vocal skill, like human language and bird songs, is underlain by learning. Vocal learning, even when occurring in adulthood, is thought to largely depend on a sensitive/critical period during postnatal development, and learned vocal patterns emerge gradually as the long-term consequence of vocal practice during this critical period. In this scenario, it is presumed that the effect of vocal practice is thus mainly limited by the intrinsic timing of age-dependent maturation factors that close the critical period and reduce neural plasticity. However, an alternative, as-yet untested hypothesis is that vocal practice itself, independently of age, regulates vocal learning plasticity. Here, we explicitly discriminate between the influences of age and vocal practice using a songbird model system. We prevented zebra finches from singing during the critical period of sensorimotor learning by reversible postural manipulation. This enabled to us to separate lifelong vocal experience from the effects of age. The singing-prevented birds produced juvenile-like immature song and retained sufficient ability to acquire a tutored song even at adulthood when allowed to sing freely. Genome-wide gene expression network analysis revealed that this adult vocal plasticity was accompanied by an intense induction of singing activity-dependent genes, similar to that observed in juvenile birds, rather than of age-dependent genes. The transcriptional changes of activity-dependent genes occurred in the vocal motor robust nucleus of the arcopallium (RA) projection neurons that play a critical role in the production of song phonology. These gene expression changes were accompanied by neuroanatomical changes: dendritic spine pruning in RA projection neurons. These results show that self-motivated practice itself changes the expression dynamics of activity-dependent genes associated with vocal learning plasticity and that this process is not tightly linked to age-dependent maturational factors.

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A quantitative method for analyzing species-specific vocal sequence pattern and its developmental dynamics

Cited by 13 publications

References 32 publications

Inter‐ and intra‐specific differences in muscarinic acetylcholine receptor expression in the neural pathways for vocal learning in songbirds

Inter‐ and intra‐specific differences in muscarinic acetylcholine receptor expression in the neural pathways for vocal learning in songbirds

Transcriptional regulatory divergence underpinning species-specific learned vocalization in songbirds

Vocal practice regulates singing activity–dependent genes underlying age-independent vocal learning in songbirds

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