Dataset Information

Brain stem feedback in a computational model of birdsong sequencing.

ABSTRACT: Uncovering the roles of neural feedback in the brain is an active area of experimental research. In songbirds, the telencephalic premotor nucleus HVC receives neural feedback from both forebrain and brain stem areas. Here we present a computational model of birdsong sequencing that incorporates HVC and associated nuclei and builds on the model of sparse bursting presented in our preceding companion paper. Our model embodies the hypotheses that 1) different networks in HVC control different syllables or notes of birdsong, 2) interneurons in HVC not only participate in sparse bursting but also provide mutual inhibition between networks controlling syllables or notes, and 3) these syllable networks are sequentially excited by neural feedback via the brain stem and the afferent thalamic nucleus Uva, or a similar feedback pathway. We discuss the model's ability to unify physiological, behavioral, and lesion results and we use it to make novel predictions that can be tested experimentally. The model suggests a neural basis for sequence variations, shows that stimulation in the feedback pathway may have different effects depending on the balance of excitation and inhibition at the input to HVC from Uva, and predicts deviations from uniform expansion of syllables and gaps during HVC cooling.

SUBMITTER: Gibb L

PROVIDER: S-EPMC2746794 | biostudies-literature | 2009 Sep

REPOSITORIES: biostudies-literature

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Brain stem feedback in a computational model of birdsong sequencing.

Gibb Leif L Gentner Timothy Q TQ Abarbanel Henry D I HD

Journal of neurophysiology 20090624 3

Uncovering the roles of neural feedback in the brain is an active area of experimental research. In songbirds, the telencephalic premotor nucleus HVC receives neural feedback from both forebrain and brain stem areas. Here we present a computational model of birdsong sequencing that incorporates HVC and associated nuclei and builds on the model of sparse bursting presented in our preceding companion paper. Our model embodies the hypotheses that 1) different networks in HVC control different sylla ...[more]

PMID: 19553477

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Project description:Accurate coordination of the sequencing and timing of motor gestures is important for the performance of complex and evolutionarily relevant behaviors. However, the degree to which motor sequencing and timing are related remains largely unknown. Birdsong is a communicative behavior that consists of discrete vocal motor elements ('syllables') that are sequenced and timed in a precise manner. To reveal the relationship between syllable sequencing and timing, we analyzed how variation in the probability of syllable transitions at branch points, nodes in song with variable sequencing across renditions, correlated with variation in the duration of silent gaps between syllable transitions ('gap durations') for adult Bengalese finch song. We observed a significant negative relationship between transition probability and gap duration: more prevalent transitions were produced with shorter gap durations. We then assessed the degree to which long-term age-dependent changes and acute context-dependent changes to syllable sequencing and timing followed this inverse relationship. Age- but not context-dependent changes to syllable sequencing and timing were inversely related. On average, gap durations at branch points decreased with age, and the magnitude of this decrease was greater for transitions that increased in prevalence than for transitions that decreased in prevalence. In contrast, there was no systematic relationship between acute context-dependent changes to syllable sequencing and timing. Gap durations at branch points decreased when birds produced female-directed courtship song compared to when they produced undirected song, and the magnitude of this decrease was not related to the direction and magnitude of changes to transition probabilities. These analyses suggest that neural mechanisms that regulate syllable sequencing could similarly control syllable timing but also highlight mechanisms that can independently regulate syllable sequencing and timing.

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Project description:The neural basis of how learned vocalizations change during development and in adulthood represents a major challenge facing cognitive neuroscience. This plasticity in the degree to which learned vocalizations can change in both humans and songbirds is linked to the actions of sex steroid hormones during ontogeny but also in adulthood in the context of seasonal changes in birdsong. We investigated the role of steroid hormone signaling in the brain on distinct features of birdsong using adult male canaries (Serinus canaria), which show extensive seasonal vocal plasticity as adults. Specifically, we bilaterally implanted the potent androgen receptor antagonist flutamide in two key brain regions that control birdsong. We show that androgen signaling in the motor cortical-like brain region, the robust nucleus of the arcopallium (RA), controls syllable and trill bandwidth stereotypy, while not significantly affecting higher order features of song such syllable-type usage (i.e., how many times each syllable type is used) or syllable sequences. In contrast, androgen signaling in the premotor cortical-like brain region, HVC (proper name), controls song variability by increasing the variability of syllable-type usage and syllable sequences, while having no effect on syllable or trill bandwidth stereotypy. Other aspects of song, such as the duration of trills and the number of syllables per song, were also differentially affected by androgen signaling in HVC versus RA. These results implicate androgens in regulating distinct features of complex motor output in a precise and nonredundant manner.SIGNIFICANCE STATEMENT Vocal plasticity is linked to the actions of sex steroid hormones, but the precise mechanisms are unclear. We investigated this question in adult male canaries (Serinus canaria), which show extensive vocal plasticity throughout their life. We show that androgens in two cortex-like vocal control brain regions regulate distinct aspects of vocal plasticity. For example, in HVC (proper name), androgens regulate variability in syntax but not phonology, whereas androgens in the robust nucleus of the arcopallium (RA) regulate variability in phonology but not syntax. Temporal aspects of song were also differentially affected by androgen signaling in HVC versus RA. Thus, androgen signaling may reduce vocal plasticity by acting in a nonredundant and precise manner in the brain.

Dataset Information

Brain stem feedback in a computational model of birdsong sequencing.

Publications

Brain stem feedback in a computational model of birdsong sequencing.

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