Relative Contribution of Proprioceptive and Vestibular Sensory Systems to Locomotion: Opportunities for Discovery in the Age of Molecular Science

Abstract

Locomotion is a fundamental animal behavior required for survival and has been the subject of neuroscience research for centuries. In terrestrial mammals, the rhythmic and coordinated leg movements during locomotion are controlled by a combination of interconnected neurons in the spinal cord, referred as to the central pattern generator, and sensory feedback from the segmental somatosensory system and supraspinal centers such as the vestibular system. How segmental somatosensory and the vestibular systems work in parallel to enable terrestrial mammals to locomote in a natural environment is still relatively obscure. In this review, we first briefly describe what is known about how the two sensory systems control locomotion and use this information to formulate a hypothesis that the weight of the role of segmental feedback is less important at slower speeds but increases at higher speeds, whereas the weight of the role of vestibular system has the opposite relation. The new avenues presented by the latest developments in molecular sciences using the mouse as the model system allow the direct testing of the hypothesis.

The role of intraspinal sensory neurons in the control of quadrupedal locomotion

“…For example, walking on a balance beam reduces lateral stability by decreasing the available base of support or walking on the horizontal ladder requires to overextend hindlimbs in order to land on the same rung where the forelimbs touched down, thus resulting in exaggerated hip torsion and spinal bending (Akay and Murray, 2021). Surprisingly we did not observe any defect in locomotor behavior upon elimination of Pkd2l1.…”

“…The regularity and precision of foot placement represent a critical feature of motor control in limbed animals (Grillner and El Manira, 2020). In particular, it is especially important for navigating the diverse terrains and obstacles animals are confronted with in the wild and 13 require dynamic integration of different sources of sensory information (Akay and Murray, 2021). Thus, our data suggests that the role of CSF-cN as a sensory system monitoring curvature of the body axis has evolved from modulation of wave-like tail movements at the basis of swimming in fish, to the control of adaptive motor responses necessary to regulate the accuracy of foot placement in limbed mammals.…”

“…Finally, we tested skilled locomotion by assessing walking on the balance beam and horizontal ladder, tasks that are known to require tactile and proprioceptive sensory feedback in order to achieve regularity and accuracy in foot placement (Akay and Murray, 2021). We used beams and ladders of different widths (2 cm and 1 cm) and rung spacing (1 cm and 2 cm) in order to assess the effect of progressively more difficult conditions (Rossignol et al, 2006).…”

Influence of controlled masticatory muscle activity on dynamic reactive balance

“…; where Each of the four perturbation directions was analysed separately for performance evaluation since postural response may differ depending on the perturbation direction. 33,[36][37][38][39] For each direction, a one-way ANOVA was performed to compare the groups' balance performances. For the segmental kinematics, a two-way ANOVA [5 ARs × 3 groups] was calculated if significant results were present at the performance level.…”

“…The four directions of perturbation were analysed independently, as suggested by Freyler et al 33 because muscle spindles provide different information dependent on the direction as well the velocity of perturbations. 39 In addition, the direction of surface translation is an important factor for the sensation, processing and output of the postural responses. 33,37 Therefore, the four directions of perturbations were treated as different tasks.…”