Distinct locomotor precursors in newborn babies

Abstract

Mature locomotion involves modular spinal drives generating a set of fundamental patterns of motoneuron activation, each timed at a specific phase of locomotor cycles and associated with a stable muscle synergy. How locomotor modules develop and to what extent they depend on prior experience or intrinsic programs remains unclear. To address these issues, we herein leverage the presence at birth of two types of locomotor-like movements, spontaneous kicking and weight-bearing stepping. The former is expressed thousands of times in utero and postnatally, whereas the latter is elicited de novo by placing the newborn on the ground for the first time. We found that the neuromuscular modules of stepping and kicking differ substantially. Neonates kicked with an adult-like number of temporal activation patterns, which lacked a stable association with systematic muscle synergies across movements. However, on the ground neonates stepped with fewer temporal patterns but all structured in stable synergies. Since kicking and ground-stepping coexist at birth, switching between the two behaviors may depend on a dynamic reconfiguration of the underlying neural circuits as a function of sensory feedback from surface contact. We tracked the development of ground-stepping in 4- to 48-mo-old infants and found that, after the age of 6 mo, the number of temporal patterns increased progressively, reaching adult-like conformation only after independent walking was established. We surmise that mature locomotor modules may derive by combining the multiple patterns of repeated kicking, on the one hand, with synergies resulting from fractionation of those revealed by sporadic weight-bearing stepping, on the other hand.

Keywords: development; modular control; pattern generation; stepping.

Fig. 1.

Recorded EMG profiles during stepping and kicking. (A) Examples of foot motion and raw EMGs in different neonates. Limb length, distance between GT and LM markers; 5MT_y, y coordinate of 5MT-marker; CL, contralateral leg muscles. Stepping includes stance and swing (vertical line marks transition). Kicking includes a flexion–extension unit (FEU) and a time-epoch just preceding and of the same duration as the FEU. Time scale for all panels in the leftmost panel. (B) Ensemble-averaged (across all cycles of all subjects of each group) rectified, filtered EMG profiles aligned with stance onset (stepping), or −100% FEU (kicking) are plotted over a normalized time base. Bottom to Top: Kicking in neonates (green), stepping at increasing treadmill speeds (grayscale). Data refer to pooled cycles from all neonates kicking supine and all children stepping on treadmill. g1, 4- to 6-mo infants; g2, 6 to 8 mo; g3, 8 to 10 mo; g4, 10 to 14 mo; g5, toddlers, 12 to 15 mo (numbers of subjects in SI Appendix, Supplementary Methods).

Fig. 2.

Relationship of EMG with speed and cycle. (A) Mean (+SD) EMG across BF, RF, LG, and TA muscles (Upper) and center of activity of average rectified EMG for LG and TA (Lower) versus treadmill speed (same speeds as in Fig. 1B, range 0.03 to 0.6 m/s). An asterisk (*) (one-way ANOVA) and pound sign (^#) (Watson–Williams multisample test for equal means) denote significant (P < 0.05) differences across speeds. (B) Polar histograms of center of activity for kicking and treadmill-stepping versus normalized cycles discretized in 20 sectors. Black arrows: Progression time, with angle that varies from 0 to 360° corresponding to 0 and 100% cycle for stepping, and to −100% and 100% FEU for kicking. Bar height denotes the percentage of cycles whose center of activity is located in the corresponding sector. Red arrows: Resultant (circular mean) center of activity (Rayleigh test for nonuniform circular distributions, P < 0.05). Data refer to pooled cycles from neonates kicking supine and children stepping on treadmill, where center of activity was identifiable (Rayleigh test, P < 0.05). In B, data from all infants of g1 to g5 were pooled together.

Fig. 3.

Cluster analysis of computed neuromuscular modules of bilateral EMGs for kicking and stepping on treadmill. (A, Upper) Clusters of activation patterns (S > 0.2) from single cycles of all subjects of each group in gray, average patterns in black. Corresponding synergies weights (S > 0.2) for single cycles in color, average values as empty bars. Patterns and synergies are plotted only if S > 0.2 in >15% of cases. (Lower) Not-clustered (nc, S ≤ 0.2) activation patterns (light gray) and associated weights. Silhouettes of activation patterns (B) and synergies weights (C) ranked in decreasing order for the single kicks or steps of A (below-threshold silhouettes in light color). Kicking cycles included −100% ÷ 100% FEU. g6, preschoolers, 24 to 48 mo.

Fig. 4.

Cluster analysis of computed neuromuscular modules for stepping on walkway at different levels of body weight supported by the neonate. Range of supported body weight (BWS) is 33 to 65% (mean = 57%, n = 85 strides), 65 to 75% (mean = 70%, n = 63 strides), and 75 to 93% (mean = 81%, n = 67 strides), from left to right. Same format as in Fig. 3A.

Fig. 5.

Cluster analysis of the activation patterns computed from the spatial decomposition of muscle activities over data ensembles in neonates. (A) Results for kicking by considering four modules. (B) Results for stepping by considering two modules. Each column plots for each module (from top to bottom) the activation patterns that fit each cluster derived from spatial decomposition, along with the corresponding percentage of cases.

Fig. 6.

Reconstruction of EMG activities of stepping children using neonate kicking patterns. Box-and-whisker plots of median and 5th to 95th percentiles (over 100 bootstrap iterations) of the VAF of the reconstruction of the EMGs of each group of children (neonates, g1 to g6); the whiskers extend to the lowest and highest values.

Fig. 7.

Muscle synergies of preschoolers explained as fractionations of synergies of ground-stepping neonates. (A) The procedure identified synergies of preschoolers as fractionations of neonate synergies in the indicated percentages, since the synergies identified as fractionations could be linearly combined to reconstruct the corresponding neonate synergies. (B) The same procedure applied to random synergies obtained by shuffling the experimental ones. (C) Box-and-whisker plots for median and 5th to 95th percentiles (over 100 bootstrap iterations) of scalar-product similarity between original and reconstructed synergies. (D) Overall percentages of neonate synergies significantly split in the synergies of preschoolers or shuffled data.