The Function of the Mammal Extrinsic Tongue Musculature in the Transition from Suckling to Drinking

Abstract

The transition from suckling to drinking is a developmental pathway that all mammals take. In both behaviors, the tongue is the primary structure involved in acquiring, transporting, and swallowing the liquid. However, the two processes are fundamentally different: during suckling, the tongue must function as a pump to generate suction to move milk, whereas during drinking, the tongue moves backwards and forwards through the mouth to acquire and move water. Despite these fundamental differences, we have little understanding of how tongues role varies between these behaviors. We used an infant pig model to investigate the relationships between anatomy, physiology, and function of the tongue to examine how lingual function is modulated in the transition from infancy to adulthood. We found that while some muscles were proportionally largest at birth, others were proportionally larger at the time of weaning. Furthermore, we found variation in tongue movements between suckling and drinking along both the mediolateral and anteroposterior axes, resulting in differences in tongue deformation between the two behaviors. The extrinsic tongue muscles also changed in function differently between drinking and suckling. Genioglossus increased its activity and turned on and off earlier in the cycle during drinking, whereas hyoglossus fired at lower amplitudes during drinking, and turned on and off later in the cycle. Together, the data highlight the significant need for high neuroplasticity in the control of the tongue at a young age in mammals and suggest that the ability to do so is key in the ontogeny and evolution of feeding in these animals.

Fig. 1

Total excursion of lateral tongue markers during bottle feeding (gold) and drinking (blue). Black lines indicate statistically significant differences between feeding modalities, gold lines indicate statistically significant differences between tongue regions during bottle feeding, blue lines indicate statistically significant differences between tongue regions during drinking. Solid lines indicate statistically significant differences with large effect sizes, dashed lines indicate statistically significant differences with medium effect sizes.

Fig. 2

Movement of the medial tongue in anterior (A, top), middle (B, middle), and posterior (C, bottom) locations. Left side indicates the mean movement of each marker in each condition ± standard error, with the start position at zero. Lines on the right plot indicate statistically significant differences between feeding conditions (solid = large effect size, dashed = medium effect size).

Fig. 3

Three-dimensional distance between the anterior and middle (A) and middle to posterior (B) medial tongue markers ± standard error, illustrating that deformation along the anteroposterior axis varies with feeding modality.

Fig. 4

Boxplots demonstrating cycle duration (left), hyoglossus firing duration (middle), and genioglossus firing duration (right) during bottle feeding (gold) and drinking (blue). Dashed lines indicate statistically significant differences with medium effect sizes.

Fig. 5

Muscle activity of the hyoglossus (left) and genioglossus (right) during bottle feeding (gold) and drinking (blue). (A) Onset relative to the beginning of the cycle, (B) offset relative to the beginning of the cycle, and (C) AUC standardized to the maximum AUC per electrode for each cycle. Lines on the right plot indicate statistically significant differences between feeding conditions (solid = large effect size, dashed = medium effect size).