Decrease in Muscle Contraction Time Complements Neural Maturation in the Development of Dynamic Manipulation

Abstract

Developmental improvements in dynamic manipulation abilities are typically attributed to neural maturation, such as myelination of corticospinal pathways, neuronal pruning, and synaptogenesis. However the contributions from changes in the peripheral motor system are less well understood. Here we investigated whether there are developmental changes in muscle activation-contraction dynamics and whether these changes contribute to improvements in dynamic manipulation in humans. We compared pinch strength, dynamic manipulation ability, and contraction time of the first dorsal interosseous muscle in typically developing preadolescent, adolescent, and young adults. Both strength and dynamic manipulation ability increased with age (p Ͻ 0.0001 and p Ͻ 0.00001, respectively). Surprisingly, adults had a 33% lower muscle contraction time compared with preadolescents (p Ͻ 0.01), and contraction time showed a significant (p Ͻ 0.005) association with dynamic manipulation abilities. Whereas decreases in muscle contraction time during development have been reported in the animal literature, our finding, to our knowledge, is the first report of this phenomenon in humans and the first finding of its association with manipulation. Consequently, the changes in the muscle contractile properties could be an important complement to neural maturation in the development of dynamic manipulation. These findings have important implications for understanding central and peripheral contributors to deficits in manipulation in atypical development, such as in children with cerebral palsy.

Immature Spinal Locomotor Output in Children with Cerebral Palsy

“…Progressive changes of gait kinematics and kinetics may depend on musculoskeletal growth (including foot shape modifications and ossification of the soft bones of the feet, Bertsch et al, 2004), development of the vestibular system (Wiener-Vacher et al, 1996), decrease of central conduction delays (Eyre et al, 1991) and muscle contraction time (Dayanidhi et al, 2013), and maturation of central neuronal pathways (Paus et al, 1999). In TD toddlers at their first unsupported steps, stable planar covariation of the limb segment angular motion (Cheron et al, 2001b), foot trajectory (Dominici et al, 2007) and pendulum-like behavior of the COM (Ivanenko et al, 2004) are still immature.…”

Sex differences in leg dexterity are not present in elite athletes

“…At this point, however, we cannot propose a definitive mechanistic link between the properties of the attractors and nature or structure of specific neuroanatomical structures or neural controllers. Future work is necessary to interpret these empirical results about leg dexterity in a mechanistic way (e.g., [27]), as we have begun to do for finger dexterity (e.g., [4, 15, 25, 34]).…”

Quantitative assessment of dynamic control of fingertip forces after pollicization

“…Outcomes after pollicization have been reported, but few studies provide prognostic guidelines for clinicians to follow in the care of these children. In addition, dexterous manipulation has a prolonged phase of improvement during childhood and adolescence [11, 12], but the impact of pollicization on the development of neural control of fingertip forces has not been elaborated. This study successfully quantifies the dynamic interaction between the magnitude and directional control of finger forces in children after pollicization and identifies differences compared to controls.…”

“…Children tend to have both higher force velocity and higher force RMS than adults (Figure 4) since they are still developing and have less robust control strategies [11, 12]. While force velocity and its variability among individuals tend to increase as RMS increases among controls, however, the variability is much greater for the pollicized hands.…”

“…The S-D test is a well-validated methodology for measuring dexterous manipulation objectively and quantitatively [10]. It has been used successfully to evaluate dexterity in healthy children [11, 12], aging [13], and adult clinical populations [14]. …”