Prenatal acoustic communication triggers adaptive vascular programming in the developing avian brain

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Abstract
Developmental plasticity allows organisms to adjust their phenotypes to match environmental conditions, but how sensory cues program specific physiological systems remains poorly understood. In Australian zebra finches, incubating parents emit heat calls during extreme temperatures, and embryos exposed to these acoustic signals develop enhanced thermal tolerance and altered growth trajectories as adults, a striking example of anticipatory programming. We hypothesized that heat call exposure alters embryonic hypothalamic gene expression, given this brain region's central role in integrating environmental signals and regulating metabolism, thermoregulation and growth. We exposed zebra finch embryos to playback of parental heat calls or control calls during late incubation and used RNA-sequencing of hypothalamic tissue to identify transcriptional responses. Contrary to predictions of widespread neuroendocrine reprogramming, heat call exposure produced targeted changes: robust downregulation of genes regulating vascular smooth muscle contraction and cytoskeletal dynamics, with coordinated isoform switching. Cell-type analyses revealed these molecular changes localized to vascular endothelial cells, smooth muscle cells and ependymal cells, the cellular components that control cerebral blood flow and regulate the brain's vascular barrier. Gene expression patterns suggest increased vascular plasticity that may protect against heat-induced cellular damage. Remarkably, these adaptive modifications occurred in response to an acoustic signal alone, without thermal exposure. Our results provide transcriptional evidence that prenatal acoustic cues may program cerebrovascular function through cell type-specific gene regulation, providing a novel mechanism for sensory-mediated developmental plasticity. This targeted vascular programming may represent a conserved strategy for anticipatory adaptation to predictable thermal challenges across endothermic vertebrates.
Funding Information
  • Australian Research Council (DP180101207)
  • Australian Research Council (DE170100824)
  • Australian Research Council (FT140100131)
  • Australian Research Council (DP210101238)
  • Biotechnology and Biological Sciences Research Council (BB/S003223/1)
  • Ministerio de Ciencia e Innovación (RYC2019-028066-I)
  • Ministerio de Ciencia e Innovación (PID2021-128494NA-I00)
  • Clemson University

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