TP, FDL, and FHL are collectively crucial role to counteracting gravity and providing functional support, as well as dynamic stabilization during locomotion [7]. Most studies on the posterior calf muscles have concentrated on the triceps hamstrings, known for producing relatively larger external torque at the ankle [3, 42]. However, there is limited anatomical research on intramuscular characteristics, analysis of muscle type-specific composition, and the corresponding causes of injuries specific to TP, FDL, and FHL. Therefore, in this study, we conducted histological measurements of these three muscles to assess significant variances in collagen concentration, elastic fiber ratio, and distinctions among muscle types, along with examining fascicle characteristics using US.
Elastic behavior, a key property of skeletal muscle, is determined by both the muscle tissue components and the connective tissue surrounding it. The connective tissue in muscles plays a vital role in transmitting and withstanding mechanic loadings during muscle activity [17]. Studies have indicated that muscles’ mechanical load-bearing characteristics vary with the collagen content [6]. Collagen, a connective tissue protein, contributes significantly to the tensile and passive viscoelastic properties of major structural muscles [22]. Cavagna’s findings (1977) suggest that the role of muscles depends on the relative amount of elastic compliance in its tendon and contractile component [10]. Excessive rigid collagenous connective tissue in strongly contracting fast muscles may hinder efficiency and the speed of contraction [11]. This underscores that elastic stiffness can be influenced by the ratio of collagen fibers within the muscle [35]. In essence, the extrinsic load and influence applied to the soles vary depending on the ratio of collagen and elastic fibers within each muscle. Data from Kovanen et al. (1980) demonstrates notable quantitative distinctions in intramuscular collagenous connective tissue between fast and slow muscles, including their respective fibers [34]. Our specific findings seem to confirm the correlation between functional contractile values and mechanical properties that affect the flexibility of skeletal muscle. This correlation is elucidated by a quantitative imbalance in the distribution ratio of collagen and elastic fibers. In this study, we histologically described the muscular characteristics of TP, FDL, and FHL (Fig. 1). Among these muscles, TP had the highest concentration of collagen. We also found the TP muscle in the posterior calf predominantly consisted of type I slow twitch muscle fibers. These histological findings carry significant implications for the functional role of the TP, which connects at the posterior calf at the sole, playing a crucial role in controlled movement and providing stability of the ankle and sole. Consistent with our findings (Figs. 1 and 3), the TP is composed primarily of slow-twitch (type I) muscle fibers and a relatively large number of collagen fibers. This composition enables sustained, prolonged contractions without fatigue, meeting the endurance demands associated with activities such as walking, standing, and maintaining posture [12]. Studies have demonstrated that slow contractile muscles, primarily responsible for postural maintenance, tend to exhibit higher collagen concentrations than do fast contractile muscles in voluntary movements [34, 38]. Furthermore, TP regulates weight distribution by controlling the subtalar joint position and determining foot flexibility through its control over the transverse tarsal joints during the gait cycle [4, 27, 41]. TP may impair the supportive function of the medial arch through repetitive stress, gradually increasing tension within surrounding muscles and ligaments, causing structural deformity and ipsilateral valgus gonarthrosis of the foot. Consequently, these alterations may disrupt the efficient mechanical pathway of the foot and negatively affect gait. The severity of these impacts can escalate to conditions like PTTD and reduced range of motion of the hallux [13, 21, 45, 53]. Theoretical implications suggest that hindfoot abduction and an increased medial longitudinal arch angle align talonavicular and calcaneocuboid joints for effective shock absorption, promoting heel elevation and generating substantial forces in the TP, FDL, and FHL to aid ankle support during the swing phase. Hence, weakening of the TP may progress sequentially and multifactorially, involving the adjacent FDL and FHL. The collective action of TP, FDL, and FHL contributes to the resistance of the subtalar joint complex on the medial malleolus of the hindfoot, supporting body weight, facilitating hindfoot stabilization, and influencing foot propulsion [60]. Tsutsumi et al. (2002) emphasize that TP, FDL, and FHL interaction contributes significantly to ankle stability during weight bearing through interactions with the joint capsular complex [55]. The TP's role is continual in regulating movement through eccentric contractions and providing essential support to the body. In clinical contexts, persistent and repetitive contraction of the TP may lead to shin splints [8]. This aligns with the notion that the slow twitch nature of the TP, which anchors the interosseous membrane, eventually exerts tension on the periosteum [57]. Recent study of Morley et al. (2019) highlight that the microscopic structure of the interosseous membrane, along with its sensory nerve endings, may contribute to proprioception in response to mechanoreceptors [43]. Consequently, as evidenced by our findings, TP, connected to the interosseous membrane and capable of maintaining constant, slow-twitch force control, is crucial to sustaining stability in the calf and sole. This emphasizes its influence on the functional mechanism of the FDL and FHL.
In relative terms, our results indicate that FDL and FHL predominantly exhibit fast twitch characteristics (Figs. 3 and 4). FDL and FHLs are believed to drive body movement by eliciting rapid plantar flexion involving the big toe and adjacent toes. FDL was confirmed to contain a relatively higher collagen content compared to FHL (Fig. 2). This suggests that FDL contributes to enhanced stability of the entire sole during the swing phase, preparing it for forward movement. Meanwhile, FHL influences the mechanical propulsion force, rapidly striking the sole in alignment with its histological characteristics. The FHL generates the highest instantaneous force among other plantar flexor muscles during the swing phase, just before toe-off. This impact indirectly can influence the function of surrounding synergistic and intrinsic muscles. Given that the FHL serves as a pivotal contributor to ankle plantar flexion, alterations in FHL function are likely to have repercussions on the performance of other plantar flexors [19]. The shifts in FHL function, as emphasized by Angin et al.’s (2014) study on flatfoot, underscore the critical importance of understanding the relative activity of the FHL in comparison to other deep plantar flexors under such conditions [2]. It stands to reason that the greater is the proportional contribution of the hallux, the greater is the intrinsic force relative to the cross-sectional area of the FHL. Generally, the peak pressure experienced by the hallux significantly surpasses the combined peak pressure of the other four phalanges [36, 54]. As age advances and with excessive overuse, collagen synthesis diminishes, giving rise to corresponding physiological and pathological alterations in elastic fibers, ultimately leading to musculoskeletal disorders [16, 56]. A biopsy study by Grimby et al. (1982) found that age-related muscle decline was associated with a more pronounced decrease in muscle fiber size for type II fibers compared to type I fibers [23]. Additionally, changes in the structural-mechanical properties of the muscles may expedite stimulation of biomechanical divergent changes in the talonavicular and calcaneocuboid joints of the feet that abnormally occur in elderly individuals due to frequent compensatory contractions of the TP, FDL, and FHL [51].
The structural properties of muscles, including thickness, fascial angle, and length, exhibit a strong correlation with maximal strength and power, typically assessed by the physiological cross-sectional area (PCSA) [1, 40]. Cross-sectional area and fascicle length notably influence the rate of muscle shortening and, consequently, its ability to generate force [32]. Hence, we conducted an analysis using US to examine the angle and length of muscle fascicles. Muscle pennation significantly contributes to transmitting forces from the contractile element to the tendon. The degree of pentation, contingent on muscle length significantly affects the moment the muscle generates at the joint [58]. While the pennation angle of the intrinsic plantar flexors beneath the foot is relatively small, without significant differences in generating force [39], our study results indicate that the pennation angle of the three long synergistic muscles passing through the ankle joint can vary in its functional role (Fig. 6 and Table 1). Moreover, our histological and muscle architectural characteristics findings may align with the force-generating capacity highlighted in existing EMG studies. The FHL also might contribute to accelerating momentarily the body [20]. EMG studies indicated that with increased gait speed, stimulation for great toe flexion surpassed total foot flexion, underscoring the heightened importance of the FHL at higher speeds [46]. However, by dispersing energy across multiple joints, FDL and FHL exhibit relatively offset mechanical output values compared to TP in terms of the maximum voluntarily produced strength of the joint moment arm [49].
It is important to acknowledge the limitations of this study. Connective tissue can influence mechanical properties through various cross-links depending on the type of collagen. Despite both types I and III collagens in muscle fibers being fibrillar, they exert similar overall effects on durability and strength [59]. Thus, considering the histologic findings and statistical consistency observed, any potential effect is anticipated to be minimal. Furthermore, the age of the cadaver from which the anatomical specimen was obtained might have influenced the results. Changes in collagen proportion within muscle composition can vary due to factors like sex, age, exercise status, pathological conditions, and muscle mass [24]. Previous studies on cadavers have highlighted the possibility of various pathological conditions associated with elastic fiber assembly in connective tissues and alterations in muscle collagen [18, 25, 50]. Another consideration is the presence of numerous intrinsic muscles contributing to maintaining posture in the feet. However, as this study is based on cadaveric specimens, it cannot provide biomechanical information on the relative maximum muscle contraction force and mechanical output during active movement. While US data on fascicle length-joint angles offer insight into living organisms, it is crucial to note that the results in this study were obtained from cadavers, which introduces the possibility of error. Therefore, verification in a clinical setting is essential for more precise validation. Ultimately, our emphasis lies in identifying differences in passive mechanical influences stemming from the intrinsic collagen-elastic fiber proportion of muscles.