Interlimb Coordination in Human Crawling Reveals Similarities in Development and Neural Control With Quadrupeds

The study of quadrupeds has furnished most of our understanding of mammalian locomotion. To allow a more direct comparison of coordination between the four limbs in humans and quadrupeds, we studied crawling in the human, a behavior that is part of normal human development and mechanically more similar to quadrupedal locomotion than is bipedal walking. Interlimb coordination during hands-and-knees crawling is compared between humans and quadrupeds and between human infants and adults. Mechanical factors were manipulated during crawling to understand the relative contributions of mechanics and neural control. Twenty-six infants and seven adults were studied. Video, force plate, and electrogoniometer data were collected. Belt speed of the treadmill, width of base, and limb length were manipulated in adults. Influences of unweighting and limb length were explored in infants. Infants tended to move diagonal limbs together (trot-like). Adults additionally moved ipsilateral limbs together (pace-like). At lower speeds, movements of the four limbs were more equally spaced in time, with no clear pairing of limbs. At higher speeds, running symmetrical gaits were never observed, although one adult galloped. Widening stance prevented adults from using the pace-like gait, whereas lengthening the hind limbs (hands-and-feet crawling) largely prevented the trot-like gait. Limb length and unweighting had no effect on coordination in infants. We conclude that human crawling shares features both with other primates and with nonprimate quadrupeds, suggesting similar underlying mechanisms. The greater restriction in coordination patterns used by infants suggests their nervous system has less flexibility

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

<p>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.</p

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

<div><p>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 <i>within</i> 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.</p></div

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).

<p>Data are as shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0148124#pone.0148124.g006" target="_blank">Fig 6</a>. 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.</p

Adaptation to treadmill speed: stride cycle modifications.

<p><b>(A)</b> 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>(B)</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 (<i>ax</i>^<i>b</i> + <i>c</i>). <b>(C)</b> Average stride duration for each successful trial; data were fit with a second order power function, as described previously [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0148124#pone.0148124.ref011" target="_blank">11</a>]. <b>(D)</b> 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).</p

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).

<p>Data are as shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0148124#pone.0148124.g004" target="_blank">Fig 4</a>. 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<0.05). BWS: Body Weight Support.</p