Gait Transitions in Human Infants: Coping with Extremes of Treadmill Speed

Abstract

Spinal pattern generators in quadrupedal animals can coordinate different forms of locomotion, like trotting or galloping, by altering coordination between the limbs (interlimb coordination). In the human system, infants have been used to study the subcortical control of gait, since the cerebral cortex and corticospinal tract are immature early in life. Like other animals, human infants can modify interlimb coordination to jump or step. Do human infants possess functional neuronal circuitry necessary to modify coordination within a limb (intralimb coordination) in order to generate distinct forms of alternating bipedal gait, such as walking and running? We monitored twenty-eight infants (7-12 months) stepping on a treadmill at speeds ranging between 0.06-2.36 m/s, and seventeen adults (22-47 years) walking or running at speeds spanning the walk-to-run transition. Six of the adults were tested with body weight support to mimic the conditions of infant stepping. We found that infants could accommodate a wide range of speeds by altering stride length and frequency, similar to adults. Moreover, as the treadmill speed increased, we observed periods of flight during which neither foot was in ground contact in infants and in adults. However, while adults modified other aspects of intralimb coordination and the mechanics of progression to transition to a running gait, infants did not make comparable changes. The lack of evidence for distinct walking and running patterns in infants suggests that the expression of different functional, alternating gait patterns in humans may require neuromuscular maturation and a period of learning post-independent walking.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Experimental setup and explanation of measures.

(A) Infants were held by an experimenter or parent in the center of the treadmill, with one leg on either side of a Plexiglas partition separating the belts. Forearm supports were provided for the person holding the infant to limit the possibility of imposing movements on the infant. (B) Stick figure showing placement of markers in infants and adults. Limb angle is defined as the angle formed between a vector from the hip to ankle and a vertical line. Positive limb angles denote limb flexion. (C) Example stride cycles with periods of double-support. Solid lines show stance phase, from foot contact (R or LFC) to toe-off (R or LTO). Spaces between lines indicate swing phase. Periods of double-support at the end of right stance are shown by grey boxes. (D) Example stride cycles with periods of flight (shown by open grey boxes).

Fig 2. Adaptation to treadmill speed: stride cycle modifications.

(A) The number of trials that were analyzed at each treadmill speed is shown by the height of each bar. Trials in which the majority of strides had a period of double support are shown in black; trials with a majority of flight strides are in white. (B) Average double support duration for each successful trial shown in (A). Negative values indicate flight. Data were fit with a second order power function (axb + c). (C) Average stride duration for each successful trial; data were fit with a second order power function, as described previously [11]. (D) Average durations of stance (black) and swing (grey) change linearly with stride duration–the slope (b) of each line is shown beside the plots. Inserted plot shows data from the highlighted region (stride duration = 0.55–1.25s; lines were re-fit to these data and recalculated slopes are shown in insert).

Fig 3. Kinematic and force data from an infant stepping at slow (A) and fast (B) speeds.

Black lines show data from right leg; grey lines show force traces from left leg. Grey boxes show the duration of right leg stance phase and white spaces in between boxes show right leg swing phase. Limb angle is defined in Fig 2. Positive limb and knee angles indicate flexion. GRF: Ground Reaction Forces; BW: Body Weight.

Fig 4. Adaptation to treadmill speed in infants and adults: changes in maximum knee flexion angle (A, B) and support length (C, D).

In infants (left column), trials in which the majority of strides had a period of double-support (DS) are in blue; trials that had mostly flight (FL) strides are in green. For adults (right column), walking and running trials are shown in blue and green, respectively. Lines were fit to each dataset, except the infant knee angle data (A), which were not significantly correlated with treadmill speed (r2 <0.03). For infant support length (C), a line was fit to all data (walking and running trials) since the correlation between treadmill speed and support length was only significant when all data were included.

Fig 5. Adaptation to treadmill speed in adults who bore 90% body weight (i.e., 10% body weight support; A, C) and 50% body weight (B, D).

Data are as shown in Fig 4. Lines were fit to each dataset when changes in the parameter (max knee flexion: A, B; support length: C, D) were significantly correlated with gait speed. Pearson correlation coefficients are reported for walking and running data in blue and green text, respectively (asterisks: p

Fig 6. Comparison between kinematic variables known to change at the adult walk-run transition.

Each infant plot (left) shows data from a subset of 10 infants who had at least one transition trial, defined as a trial in which 30–70% of strides had a period of flight. Double-support (DS-blue) and flight (FL-green) strides were averaged separately. Adult plots (right) show data from 6 adults who walked (blue) and ran (green) at the same speed (2.0m/s). (A) Top: averaged limb angle traces (± SEM across infants) for DS/walking and FL/running strides (foot-contact to foot-contact; normalized to the same cycle duration). Bottom: averaged maximum limb flexion, extension, and range of motion (* p<0.05). (B) Knee angle is expressed as degrees of flexion (0° = straight leg). Data are as shown in (A). (C) Hip height was used as an estimate of Center of Mass (CoM).

Fig 7. Changes in kinematic variables at the walk-to-run transition in adults who bore 90% body weight (i.e., 10% body weight support; left column) and 50% body weight (right column).

Data are as shown in Fig 6. Asterisks (*) show significant main effects for gait (walk versus run) for each measure; hash marks (#) show significant main effects for body weight support (10% versus 50%). BWS: Body Weight Support.