Elska B Kaczmarek, Hannah E Shideler, Skyler M Wallace, Dylan J Anderson, Emily C Volpe, Maressa E Kennedy, Harlow I Smith, Ani E Smith, Thomas H Stroud, Christopher J Mayerl
{"title":"Evaluating the impact of nipple design on tongue function in infant feeding using a dynamic endocast.","authors":"Elska B Kaczmarek, Hannah E Shideler, Skyler M Wallace, Dylan J Anderson, Emily C Volpe, Maressa E Kennedy, Harlow I Smith, Ani E Smith, Thomas H Stroud, Christopher J Mayerl","doi":"10.1093/icb/icaf130","DOIUrl":null,"url":null,"abstract":"<p><p>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.</p>","PeriodicalId":54971,"journal":{"name":"Integrative and Comparative Biology","volume":" ","pages":""},"PeriodicalIF":2.2000,"publicationDate":"2025-07-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Integrative and Comparative Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/icb/icaf130","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"ZOOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
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.
期刊介绍:
Integrative and Comparative Biology ( ICB ), formerly American Zoologist , is one of the most highly respected and cited journals in the field of biology. The journal''s primary focus is to integrate the varying disciplines in this broad field, while maintaining the highest scientific quality. ICB''s peer-reviewed symposia provide first class syntheses of the top research in a field. ICB also publishes book reviews, reports, and special bulletins.