Muscle architecture dynamics modulate performance of the superficial anterior temporalis muscle during chewing in capuchins

Abstract

Jaw-muscle architecture is a key determinant of jaw movements and bite force. While static length-force and force-velocity relationships are well documented in mammals, architecture dynamics of the chewing muscles and their impact on muscle performance are largely unknown. We provide novel data on how fiber architecture of the superficial anterior temporalis (SAT) varies dynamically during naturalistic feeding in tufted capuchins (Sapajus apella). We collected data on architecture dynamics (changes in muscle shape or the architectural gear ratio) during the gape cycle while subjects fed on foods of different mechanical properties. Architecture of the SAT varied with phases of the gape cycle, but gape distance accounted for the majority of dynamic changes in architecture. In addition, lower gear ratios (low muscle velocity relative to fascicle velocity) were observed when animals chewed on more mechanically resistant foods. At lower gear ratios, fibers rotated less during shortening resulting in smaller pinnation angles, a configuration that favors increased force production. Our results suggest that architectural dynamics may influence jaw-muscle performance by enabling the production of higher bite forces during the occlusal phase of the gape cycle and while processing mechanically challenging foods.

Figure 1

Schematic of changes in architectural gear ratio (AGR) and muscle bulging of the temporalis in sagittal and coronal planes from scaled CT images. The red lines represent the original position of the muscle and fascicle before shortening. At high gear ratios, the increase in pinnation during shortening results in increased muscle anteroposterior thickness (anteroposterior expansion shown in sagittal view, black arrows). At low gear ratios, pinnation angle decreases and muscle mediolateral width increases (mediolateral expansion shown in coronal view, black arrows). The shaded ellipse shown in sagittal view represents the tendinous sheath.

Figure 2

(A) Anterior view of a coronal section of a capuchin right temporalis. In this study, tantalum beads were sutured at the ends of a single fascicle at its central myotendinous junction (CMJ; 1) and its superficial termination at the temporal fascia (2). A third marker was placed at the temporal fascia line roughly in the same coronal plane as the fascicle (3). The SAT fascicles are oblique to coronal and sagittal planes (cf. Fig. 1). (B) Coronal view from a CT scan of a subject animal showing the positions of each of the muscle beads (1–3) and the positioning of the tip of the coronoid process (4), which was used to measure whole-muscle length. (C) Sagittal view of a CT scan of a subject animal showing the positioning of the muscle markers (1–3) and the positioning of the tip of the coronoid process (4).

Figure 3

Averages of 30-33 gape cycles (93 total) from the three subject animals. (A) Gape distance and (B) fascicle distance, over the standardized gape cycle: maximum gape occured at the FO/FC transition, minimum gape at the SC/SO transition. Sagittal (C) and coronal (D) fascicle angles changed over the gape cycle. The largest sagittal and coronal fascicle angles occured at minimum gape; the smallest occured at maximum gape. Sagittal fascicle angle changed approximately twice as much as coronal fascicle angle over the gape cycle. The timing of minimum sagittal and coronal fascicle angles did not signficantly differ between food types. (E) LOESS fit (with a 25% smoothing span) of fascicle length velocity during the gape cycle. Fascicles shortened to the SC/SO transition (minimum gape), with the maximum shortening velocity around the FC/SC transition and maximum lengthening velocity around the SO/FO transition. (F) LOESS fit (with a 25% smoothing span) of muscle length velocity during the gape cycle. Maximum shortening velocity occurred around the FC/SC, minimum lengthening velocity occurred around the SO/FO transition. Figure generated in R (2017; https://www.R-project.org).

Figure 4

(A) Coronal and (B) sagittal fascicle angles decreased with gape distance. The slopes of these relationships varied with food mechanical properties. (C) The superficial anterior temporalis architectural gear ratio (SAT AGR) decreased with normalized gape distance until about halfway to maximum gape, i.e., the FC/SC transition. Following the halfway point, SAT AGR increased. Figure generated in R (2017; https://www.R-project.org).

Figure 5

Architectural gear ratios (AGR) varied across the gape cycle. Across the entire gape cycle (A) AGR values decreased during jaw closing until the FC/SC transition and increased throughout SC. During jaw opening, AGR values decreased until the SO/FO transition and increased during FO. Across the entire gape cycle, gape-controlled AGR (B) had a single peak at the SC/SO transition. Figure generated in R (2017; https://www.R-project.org).

Figure 6

(A) Superficial anterior temporalis architectural gear ratios (SAT AGR) were lower during the gape cycle, and (B) sagittal pinnation angles were smaller, when subject animals fed on more mechanically challenging food items. The upper and lower bounds of the boxes correspond with the 25th and 75th percentiles and the whiskers extend 1.5 times the interquartile range in either direction. The median is represented by a horizontal line inside the boxes. A significance level, p < 0.01, is indicated by three asterisks. Figure generated in R (2017; https://www.R-project.org).