Graïc Jean-Marie, Corain Livio, Finos Livio, Vadori Valentina, Grisan Enrico, Gerussi Tommaso, Orekhova Ksenia, Centelleghe Cinzia, Cozzi Bruno, Peruffo Antonella
Department of Comparative Biomedicine and Food Science, University of Padova, Legnaro, Italy.
Department of Management and Engineering, University of Padova, Vicenza, Italy.
Front Neuroanat. 2024 Jan 5;17:1330384. doi: 10.3389/fnana.2023.1330384. eCollection 2023.
The auditory system of dolphins and whales allows them to dive in dark waters, hunt for prey well below the limit of solar light absorption, and to communicate with their conspecific. These complex behaviors require specific and sufficient functional circuitry in the neocortex, and vicarious learning capacities. Dolphins are also precocious animals that can hold their breath and swim within minutes after birth. However, diving and hunting behaviors are likely not innate and need to be learned. Our hypothesis is that the organization of the auditory cortex of dolphins grows and mature not only in the early phases of life, but also in adults and aging individuals. These changes may be subtle and involve sub-populations of cells specificall linked to some circuits.
In the primary auditory cortex of 11 bottlenose dolphins belonging to three age groups (calves, adults, and old animals), neuronal cell shapes were analyzed separately and by cortical layer using custom computer vision and multivariate statistical analysis, to determine potential minute morphological differences across these age groups.
The results show definite changes in interneurons, characterized by round and ellipsoid shapes predominantly located in upper cortical layers. Notably, neonates interneurons exhibited a pattern of being closer together and smaller, developing into a more dispersed and diverse set of shapes in adulthood.
This trend persisted in older animals, suggesting a continuous development of connections throughout the life of these marine animals. Our findings further support the proposition that thalamic input reach upper layers in cetaceans, at least within a cortical area critical for their survival. Moreover, our results indicate the likelihood of changes in cell populations occurring in adult animals, prompting the need for characterization.
海豚和鲸鱼的听觉系统使它们能够在黑暗的水域中潜水,在太阳光吸收极限以下的深度捕食猎物,并与同类进行交流。这些复杂的行为需要新皮层中特定且足够的功能电路以及替代性学习能力。海豚也是早熟的动物,出生后几分钟就能屏住呼吸并游泳。然而,潜水和捕食行为可能并非天生,而是需要学习。我们的假设是,海豚听觉皮层的组织不仅在生命早期阶段生长和成熟,在成年和衰老个体中也是如此。这些变化可能很细微,涉及与某些电路特别相关的细胞亚群。
在11只宽吻海豚的初级听觉皮层中,这些海豚分属三个年龄组(幼崽、成年海豚和老年海豚),使用定制的计算机视觉和多元统计分析分别并按皮层层分析神经元细胞的形状,以确定这些年龄组之间潜在的微小形态差异。
结果显示中间神经元有明显变化,其特征是形状主要为圆形和椭圆形,主要位于皮层上层。值得注意的是,新生海豚的中间神经元表现出聚集且较小的模式,在成年后发展成更分散、形状更多样的一组。
这种趋势在老年动物中持续存在,表明这些海洋动物一生中连接在持续发展。我们的研究结果进一步支持了这样的观点,即丘脑输入到达鲸类动物的上层,至少在对它们生存至关重要的皮层区域内是这样。此外,我们的结果表明成年动物的细胞群体可能发生变化,这促使需要进行特征描述。