Doñana Biological Station EBD-CSIC, 41092 Seville, Spain.
School of Life and Environmental Sciences, Deakin University, Geelong, VIC 3216, Australia.
J Exp Biol. 2024 Mar 7;227(Suppl_1). doi: 10.1242/jeb.246696.
In recent years, the impact of prenatal sound on development, notably for programming individual phenotypes for postnatal conditions, has increasingly been revealed. However, the mechanisms through which sound affects physiology and development remain mostly unexplored. Here, I gather evidence from neurobiology, developmental biology, cellular biology and bioacoustics to identify the most plausible modes of action of sound on developing embryos. First, revealing often-unsuspected plasticity, I discuss how prenatal sound may shape auditory system development and determine individuals' later capacity to receive acoustic information. I also consider the impact of hormones, including thyroid hormones, glucocorticoids and androgen, on auditory plasticity. Second, I review what is known about sound transduction to other - non-auditory - brain regions, and its potential to input on classical developmental programming pathways. Namely, the auditory pathway has direct anatomical and functional connectivity to the hippocampus, amygdala and/or hypothalamus, in mammals, birds and anurans. Sound can thus trigger both immediate and delayed responses in these limbic regions, which are specific to the acoustic stimulus and its biological relevance. Third, beyond the brain, I briefly consider the possibility for sound to directly affect cellular functioning, based on evidence in earless organisms (e.g. plants) and cell cultures. Together, the multi-disciplinary evidence gathered here shows that the brain is wired to allow multiple physiological and developmental effects of sound. Overall, there are many unexplored, but possible, pathways for sound to impact even primitive or immature organisms. Throughout, I identify the most promising research avenues for unravelling the processes of acoustic developmental programming.
近年来，产前声音对发育的影响，尤其是对编程个体表型以适应产后环境的影响，越来越受到关注。然而，声音影响生理和发育的机制在很大程度上仍未得到探索。在这里，我从神经生物学、发育生物学、细胞生物学和生物声学收集证据，以确定声音对发育中的胚胎最可能的作用模式。首先，揭示了通常未被察觉的可塑性，我讨论了产前声音如何塑造听觉系统的发育，并决定个体以后接收声信息的能力。我还考虑了激素，包括甲状腺激素、糖皮质激素和雄激素，对听觉可塑性的影响。其次，我回顾了关于声音向其他非听觉脑区的转导及其对经典发育编程途径的潜在影响的知识。即，在哺乳动物、鸟类和无尾两栖类中，听觉通路与海马体、杏仁核和/或下丘脑具有直接的解剖学和功能连接。因此，声音可以在这些边缘区域引发即时和延迟反应，这些反应是特定于声刺激及其生物学相关性的。第三，超越大脑，我简要考虑了声音直接影响细胞功能的可能性，这基于无耳生物（如植物）和细胞培养的证据。综上所述，这里收集的多学科证据表明，大脑允许声音对生理和发育产生多种影响。总的来说，声音可能有许多未被探索但可能的途径来影响即使是原始或不成熟的生物体。在整个过程中，我确定了最有前途的研究途径，以揭示声学发育编程的过程。
