Control of Forelimb and Hindlimb Movements and Their Coordination during Quadrupedal Locomotion across Speeds in Adult Spinal Cats

Abstract

Coordinating the four limbs is critical for terrestrial mammalian locomotion. Thoracic spinal transection abolishes neural communication between the brain and spinal networks controlling hindlimb/leg movements. Several studies have shown that animal models of spinal transection (spinalization), such as mice, rats, cats, and dogs recover hindlimb locomotion with the forelimbs stationary or suspended. We know less on the ability to generate quadrupedal locomotion after spinal transection, however. We collected kinematic and electromyography data in four adult cats during quadrupedal locomotion at five treadmill speeds before (intact cats) and after low-thoracic spinal transection (spinal cats). We show that adult spinal cats performed quadrupedal treadmill locomotion and modulated their speed from 0.4 m/sec to 0.8 m/sec but required perineal stimulation. During quadrupedal locomotion, several compensatory strategies occurred, such as postural adjustments of the head and neck and the appearance of new coordination patterns between the forelimbs and hindlimbs, where the hindlimbs took more steps than the forelimbs. We also observed temporal changes, such as shorter forelimb cycle/swing durations and shorter hindlimb cycle/stance durations in the spinal state. Forelimb double support periods occupied a greater proportion of the cycle in the spinal state, and hindlimb stride length was shorter. Coordination between the forelimbs and hindlimbs was weakened and more variable in the spinal state. Changes in muscle activity reflected spatiotemporal changes in the locomotor pattern. Despite important changes in the pattern, our results indicate that biomechanical properties of the musculoskeletal system play an important role in quadrupedal locomotion and offset some of the loss in neural communication between networks controlling the forelimbs and hindlimbs after spinal transection.

Keywords: central pattern generator; interlimb coordination; locomotion; somatosensory feedback; spinal transection.

FIG. 1.

Postural adjustments during quadrupedal locomotion in adult spinal cats. (A) Superimposed silhouettes for each cat in the intact and spinal states at (1) right forelimb liftoff, right forelimb midswing and (3) right forelimb liftoff. (B) Stance phases during quadrupedal locomotion in the intact and spinal states at 0.4 m/sec for Cat 3 and Cat 1. RFL, right forelimb; RHL, right hindlimb; LFL, left forelimb; LHL, left hindlimb.

FIG. 2.

Temporal adjustments during quadrupedal locomotion in the intact and spinal states across speeds. Each panel shows cycle, stance, and swing durations during quadrupedal locomotion in the intact and spinal states at five treadmill speeds for the forelimbs (FL) (A) and the hindlimbs (HL) (B). Stance proportions (C) and double support periods (D) for the forelimbs and hindlimbs in the intact and spinal states at five treadmill speeds. At each speed, we averaged 4–42 (14.53 ± 7.74) cycles per cat. Each data point or bar is the mean ± standard deviation for the group (n = 4 cats). The p values comparing state and speeds are indicated (main effects of repeated measures analysis of variance.

FIG. 3.

Spatial adjustments during quadrupedal locomotion in the intact and spinal states across speeds. Step length (A), stride length (B), and the horizontal distances at liftoff/contact (C) during quadrupedal locomotion in the intact and spinal states at five treadmill speeds for the forelimbs (top panels) and hindlimbs (bottom panels). At each speed, we averaged 4–42 (14.53 ± 7.74) cycles per cat. Each data point or bar is the mean ± standard deviation for the group (n = 4 cats). The p values comparing state and speeds are indicated (main effects of repeated measures analysis of variance). Vertical dashed lines in C indicate the zero or shoulder/hip position.

FIG. 4.

Homolateral limb interference during quadrupedal locomotion in the intact and spinal states across speeds. Each panel shows horizontal distances between the homolateral forelimbs (FL) and hindlimbs (HL) at contact (left) and liftoff (right) of the forelimbs (top panels) and hindlimbs (bottom panels) during quadrupedal locomotion in the intact and spinal state at five treadmill speeds. At each speed, we averaged 4–42 (14.53 ± 7.74) cycles per cat. Each data point is the mean ± standard deviation for the group (n = 4 cats). The p values comparing state and speeds are indicated (main effects of repeated measures analysis of variance).

FIG. 5.

Quadrupedal locomotion in the intact and spinal states at 0.4 m/sec and 0.8 m/sec speed. Top and bottom panels show electromyography activity from selected forelimb and hindlimb muscles along with stance phases (thick horizontal lines) of the left (L) and right (R) limbs in two cats in the intact and spinal states during quadrupedal locomotion. TRI, triceps brachii; BB, biceps brachii; SOL, soleus; BFA, biceps femoris anterior; VL, vastus lateralis.

FIG. 6.

Modulation of electromyography burst durations during quadrupedal locomotion in the intact and spinal states across speeds. The figure shows burst durations in selected muscles during quadrupedal locomotion in the intact and spinal states at five treadmill speeds. At each speed, we averaged 4–42 (14.53 ± 7.74) cycles per cat. Each data point is the mean ± standard deviation for the group. The p values comparing state and speeds are indicated (main effects of repeated measures analysis of variance). BB, biceps brachii (n = 3–4 cats); TRI, triceps brachii (n = 3 cats); BFA, biceps femoris (n = 3 cats); VL, vastus lateralis (n = 3 cats); LG, lateral gastrocnemius (n = 3 cats); SOL, soleus (n = 4 cats); SRT, sartorius anterior (n = 3 cats); BFP, biceps femoris posterior (n = 3 cats).

FIG. 7.

Modulation of electromyography phasing during quadrupedal locomotion in the intact and spinal states across speeds. The figure shows burst onsets and offsets from selected muscles in a normalized cycle during quadrupedal locomotion in the intact and spinal states at five treadmill speeds. At each speed, we averaged 4–42 (14.53 ± 7.74) cycles per cat. The bars represent stance durations while the circles represent bursts onsets and offsets for the group. Each data point is the mean ± standard deviation for the group (n = 3–4 cats). P values comparing state and speeds are indicated (main effects of repeated measures analysis of variance). BB, biceps brachii (n = 4 cats); TRI, triceps brachii (n = 3 cats); BFA, biceps femoris (n = 3 cats); VL, vastus lateralis (n = 3 cats); LG, lateral gastrocnemius (n = 3 cats); SOL, soleus (n = 4 cats); SRT, sartorius anterior (n = 3 cats); BFP, biceps femoris posterior (n = 3 cats).

FIG. 8.

Step-by-step phasing of homolateral and diagonal limb pairs during tied-belt quadrupedal locomotion in two cats in the intact and spinal states at 0.4 m/sec and 0.8 m/sec. In the circular plots, phase intervals are expressed in degrees around the circumference, whereas cycle durations are plotted in radii. Each data point represents a locomotor cycle from one session in a single cat in the intact and spinal states. Only cycles with 1:1 fore-hind coordination are shown.

FIG. 9.

Interlimb coordination during quadrupedal locomotion in the intact and spinal states across speeds. Forelimb (A), hindlimb (B), homolateral (C), and diagonal (D) couplings are shown during quadrupedal locomotion in the intact and spinal states at five treadmill speeds. At each speed, we averaged 4–42 (14.53 ± 7.74) cycles per cat. Each data point is the mean ± standard deviation for the group (n = 4 cats). The p values comparing state and speeds are indicated (main effects of repeated measures analysis of variance).

FIG. 10.

Variations in interlimb coordination during quadrupedal locomotion in the intact and spinal states across speeds. Coefficients of variation of forelimb (A), hindlimb (B), homolateral (C), and diagonal (D) couplings are shown during quadrupedal locomotion in the intact and spinal states at five treadmill speeds. At each speed, we averaged 4–42 (14.53 ± 7.74) cycles per cat. Each data point is the mean ± standard deviation for the group (n = 4 cats). The p values comparing state and speeds are indicated (main effects of repeated measures analysis of variance).