Stumbling corrective reaction elicited by mechanical and electrical stimulation of the saphenous nerve in walking mice

Abstract

The ability to walk around in a natural environment requires the capacity to cope with unexpected obstacles that may disrupt locomotion. One such mechanism is called the stumbling corrective reaction (SCR) that enables animals to step over obstacles that would otherwise disturb the progression of swing movement. Here we use motion analysis and physiological recording techniques to describe the SCR in mice. We show that SCR can be elicited consistently in mice during locomotion by inserting an obstacle along the path of leg movement during swing phase. Furthermore, we show that the same behavior can be elicited if the saphenous nerve, a cutaneous nerve that would detect contact of the leg with an object, is stimulated electrically. This suggests that cutaneous afferent feedback is sufficient to elicit SCR. We further show that the SCR is phase dependent, occurring only with stimulation during swing phase, but not during early stance. During SCR elicited by either method, the foot is lifted higher to clear the object by flexing the knee, via the semitendinosus muscle, and ankle joint, by tibialis anterior contraction. The tibialis anterior also exhibits a brief extension before flexion onset. Our data provide a detailed description of SCR in mice and will be crucial for future research that aims to identify the interneurons of the premotor network controlling SCR and its neuronal mechanisms by combining motion analysis, electrophysiology and mouse genetics.

Modular organization of murine locomotor pattern in the presence and absence of sensory feedback from muscle spindles

“…First, they freely walked at a fixed speed of 0.2 m/s on a custom treadmill (workshop of the Zoological Institute, University of Cologne) for a variable amount of time, depending on each animal's will to walk. After the recordings during walking, 11 of each of the WT and Egr3 −/− mice were placed in a tank filled with water at a temperature of circa 24 °C for around 120 s. A second group (henceforth GR2) of 4 WT and 5 mutants walked on the treadmill at 0.3 m/s while one step was perturbed every second by stimulating the saphenous nerve electrically (five 0.2 ms impulses at 500 Hz), which elicited a stumbling corrective reaction (SCR; Mayer & Akay, ). Given that the stimulations were initiated at fixed time points (i.e.…”

“…every second), they occurred at random phases of the gait cycle. The strength of the stimulation was set to be 1.2× the current that was necessary to elicit the slightest response in the tibialis anterior muscle during resting, which varied between 96 and 1200 μA from animal to animal (Mayer & Akay, ). These frequent SCRs caused the mice to walk cautiously, and therefore we called these trials ‘cautious walking’.…”

“…). With the third task we applied electrical stimulation to the saphenous nerve at regular intervals in order to elicit a cautious form of walking between two consecutive stimulations (Mayer & Akay, ). We extracted synergies using non‐negative matrix factorization (NMF) (Lee & Seung, ; Santuz et al .…”

Modular organization of the murine locomotor pattern in presence and absence of sensory feedback from muscle spindles

“…Given that muscle spindles in Egr3 -/mice regress immediately after birth (20,54), we cannot exclude a certain amount of long-term adaptation in the modular control of the locomotor patterns. Nevertheless, we speculate that an acute removal of muscle spindles (8) in the adult mouse could alter the locomotor pattern in an even more amplified fashion.…”

Connecting the micro with the macro level in motor control: unravelling general sensory influences on leg stepping

“…They specify the detailed role of muscle spindle feedback by challenging the robustness of the motor output generated against perturbations. To do so, they perturb walking by electrical stimulations of the saphenous nerve that elicit stumbling corrective reactions (Mayer and Akay, ) causing the animal to exert a more cautious walking in between the stimulations. Finally, the authors test for the potential compensatory role of force feedback from Golgi tendon organs in the Egr3 −/− mice by monitoring muscle activity during swimming, a situation, in which feedback from these afferents is reduced due to the lower gravitational load induced by buoyancy.…”