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Vocal learning and flexible rhythm pattern perception are linked: Evidence from songbirds.

ABSTRACT: Rhythm perception is fundamental to speech and music. Humans readily recognize a rhythmic pattern, such as that of a familiar song, independently of the tempo at which it occurs. This shows that our perception of auditory rhythms is flexible, relying on global relational patterns more than on the absolute durations of specific time intervals. Given that auditory rhythm perception in humans engages a complex auditory-motor cortical network even in the absence of movement and that the evolution of vocal learning is accompanied by strengthening of forebrain auditory-motor pathways, we hypothesize that vocal learning species share our perceptual facility for relational rhythm processing. We test this by asking whether the best-studied animal model for vocal learning, the zebra finch, can recognize a fundamental rhythmic pattern-equal timing between event onsets (isochrony)-based on temporal relations between intervals rather than on absolute durations. Prior work suggests that vocal nonlearners (pigeons and rats) are quite limited in this regard and are biased to attend to absolute durations when listening to rhythmic sequences. In contrast, using naturalistic sounds at multiple stimulus rates, we show that male zebra finches robustly recognize isochrony independent of absolute time intervals, even at rates distant from those used in training. Our findings highlight the importance of comparative studies of rhythmic processing and suggest that vocal learning species are promising animal models for key aspects of human rhythm perception. Such models are needed to understand the neural mechanisms behind the positive effect of rhythm on certain speech and movement disorders.

SUBMITTER: Rouse AA

PROVIDER: S-EPMC8307534 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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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Vocal learning and flexible rhythm pattern perception are linked: Evidence from songbirds.

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