Speed-Dependent Modulation of the Locomotor Behavior in Adult Mice Reveals Attractor and Transitional Gaits

Abstract

Locomotion results from an interplay between biomechanical constraints of the muscles attached to the skeleton and the neuronal circuits controlling and coordinating muscle activities. Quadrupeds exhibit a wide range of locomotor gaits. Given our advances in the genetic identification of spinal and supraspinal circuits important to locomotion in the mouse, it is now important to get a better understanding of the full repertoire of gaits in the freely walking mouse. To assess this range, young adult C57BL/6J mice were trained to walk and run on a treadmill at different locomotor speeds. Instead of using the classical paradigm defining gaits according to their footfall pattern, we combined the inter-limb coupling and the duty cycle of the stance phase, thus identifying several types of gaits: lateral walk, trot, out-of-phase walk, rotary gallop, transverse gallop, hop, half-bound, and full-bound. Out-of-phase walk, trot, and full-bound were robust and appeared to function as attractor gaits (i.e., a state to which the network flows and stabilizes) at low, intermediate, and high speeds respectively. In contrast, lateral walk, hop, transverse gallop, rotary gallop, and half-bound were more transient and therefore considered transitional gaits (i.e., a labile state of the network from which it flows to the attractor state). Surprisingly, lateral walk was less frequently observed. Using graph analysis, we demonstrated that transitions between gaits were predictable, not random. In summary, the wild-type mouse exhibits a wider repertoire of locomotor gaits than expected. Future locomotor studies should benefit from this paradigm in assessing transgenic mice or wild-type mice with neurotraumatic injury or neurodegenerative disease affecting gait.

Loss of Dcc in the spinal cord is sufficient to cause a deficit in lateralized motor control and the switch to a hopping gait

“…The lower slopes of the regression lines in HoxB8-Cre; Dcc Flox/Flox and HoxB8-Cre; Dcc Flox/mutants indicate that the mutants were unable to increase their stride length as much as control mice to achieve a higher speed, likely due to the physical limitation of their hopping gait, which is different from the bounding or galloping of control animals at high speeds. (Lemieux et al, 2016). The bound/gallop we observed in the mutants is slower than that of controls and is likely due to a lack in both coordination and sufficient force among limbs and joints required for the longstride bound/gallop at high speeds seen in control animals.…”

Central control of interlimb coordination and speed‐dependent gait expression in quadrupeds

“…Similar changes were observed in real locomotion (Lemieux et al . ). Note that fore–hind asymmetries in drive weights (see Table ) created the asymmetric homolateral phase differences during bound and thus the correct extension phase sequence.…”

“…; Bellardita & Kiehn, ; Lemieux et al . ). The neural mechanisms involved in speed‐dependent gait expression are poorly understood.…”

Midbrain circuits that set locomotor speed and gait selection

“…1i, blue) and all gaits including the alternating gaits walk and trot and synchronous gaits like gallop and bound (Fig. 1e, j –upper panel) 1,17,18 . The onset of locomotion was in the range of 100–150 ms (Extended Data Fig.…”