Kaczmarek Elska B, Shideler Hannah E, Wallace Skyler M, Anderson Dylan J, Volpe Emily C, Kennedy Maressa E, Smith Harlow I, Smith Ani E, Stroud Thomas H, Mayerl Christopher J
Department of Biological Sciences, Northern Arizona University; Flagstaff, AZ.
Integr Comp Biol. 2025 Jul 12. doi: 10.1093/icb/icaf130.
The mammalian tongue is a muscular hydrostat composed of multiple muscles, each with complex fiber architecture and small motor units. This allows it to move and deform in three dimensions (3D) to function in several complex behaviors, including suckling. The ability of infant mammals to successfully suckle is dependent on these variable deformations, as the tongue must perform multiple functions simultaneously. The lateral margins of the tongue curl to seal around a nipple, while the middle of the tongue moves in an anteroposterior wave to suck milk into the mouth, transport it posteriorly, and swallow it. The kinematics, mechanics, and coordination of the tongue during suckling are impacted by nipple properties, as evidenced by differences between feeding from nipples with narrow ducts (e.g., breastfeeding) and nipples that are hollow cisterns (e.g., bottle feeding). These structural differences result in different feeding outcomes, yet their effect on tongue function and kinematics is poorly understood. In addition, despite the 3D shape of the tongue during suckling, measurements of tongue movement have been limited to motion along the midsagittal plane and have not assessed suck volume. To evaluate how tongue function differs between ducted and cisternic nipples, we used X-ray Reconstruction of Moving Morphology (XROMM) and a dynamic endocast, synchronized with intraoral suction, to quantify 3D tongue kinematics and suck volume. We found that pigs generated less suction but had greater suck volumes when they fed on cisternic nipples compared to ducted nipples. This is likely because the pigs compressed the cisternic nipple to express milk, resulting in higher flow, which we hypothesize slowed the accumulation of suction and permitted the tongue to achieve a larger suck volume. These results suggest that nipple design impacts the relationship between fluid dynamics and tongue function during feeding. In addition, we found that infants moved the surface of their tongue ventrally and posteriorly throughout the suck, but they did not increase the width of the suck volume. The use of a digital endocast to measure suck volume represents an important advance in our ability to evaluate the mechanics of feeding and could be used in the future to understand the relationships between tongue function and performance as infants mature, as well as in a comparative framework.
哺乳动物的舌头是一种由多块肌肉组成的肌肉静力学器官，每块肌肉都有复杂的纤维结构和小型运动单位。这使得舌头能够在三维空间中移动和变形，以执行多种复杂行为，包括哺乳。幼年哺乳动物成功哺乳的能力取决于这些可变的变形，因为舌头必须同时执行多种功能。舌头的外侧边缘卷曲以围绕乳头密封，而舌头中部则以前后波的形式移动，将乳汁吸入口腔，向后运输并吞咽。乳头的特性会影响哺乳期间舌头的运动学、力学和协调性，从狭窄导管乳头（如母乳喂养）和中空贮乳器乳头（如奶瓶喂养）的喂养差异中可见一斑。这些结构差异导致不同的喂养结果，但其对舌头功能和运动学的影响却知之甚少。此外，尽管哺乳时舌头呈三维形状，但对舌头运动的测量仅限于沿矢状面的运动，且未评估吸吮量。为了评估导管乳头和贮乳器乳头之间舌头功能的差异，我们使用了运动形态X射线重建技术（XROMM）和动态内铸模型，并与口腔内吸力同步，以量化舌头的三维运动学和吸吮量。我们发现，与导管乳头相比，猪在使用贮乳器乳头喂养时产生的吸力较小，但吸吮量较大。这可能是因为猪挤压贮乳器乳头以挤出乳汁，导致流速更高，我们推测这减缓了吸力的积累，并使舌头能够实现更大的吸吮量。这些结果表明，乳头设计会影响喂养过程中流体动力学与舌头功能之间的关系。此外，我们发现婴儿在整个吸吮过程中会将舌头表面向腹侧和后侧移动，但他们并没有增加吸吮量的宽度。使用数字内铸模型来测量吸吮量代表了我们评估喂养力学能力的一项重要进展，未来可用于了解婴儿成熟过程中舌头功能与表现之间的关系，以及在比较框架中的应用。
