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

From swimming to walking and flying, animals have evolved specific locomotor strategies to thrive in different habitats. All types of locomotion depend on integration of motor commands and sensory information to generate precise movements. Cerebrospinal fluid-contacting neurons (CSF-cN) constitute a vertebrate sensory system that monitors CSF composition and flow. In fish, CSF-cN modulate swimming activity in response to changes in pH and bending of the spinal cord, yet their role in higher vertebrates remains unknown. We used mouse genetics to study their function in quadrupedal locomotion and found that CSF-cN are directly integrated into spinal motor circuits by forming connections with motor neurons and premotor interneurons. Elimination of CSF-cN selectively perturbs the accuracy of foot placement required for skilled movements at the balance beam and horizontal ladder. These results identify an important role for mouse CSF-cN in adaptive motor control and indicate that this sensory system evolved a novel function from lower vertebrates to accommodate the biomechanical requirements of terrestrial locomotion.

The effect of constraining mediolateral ankle moments and foot placement on the use of the counter-rotation mechanism during walking

Stability during walking can be maintained by shifts of the Center of Pressure through modulation of foot placement and ankle moments (CoP-mechanism). An additional mechanism to stabilize gait, is the counter-rotation mechanism i.e. changing the angular momentum of segments around the Center of Mass (CoM) to change the direction of the ground reaction force. It is unknown if and how humans use the counter-rotation mechanism to control the CoM during walking and how this interacts with the CoP-mechanism. Thirteen healthy adults walked on a treadmill, while full-body kinematic and force plate data were obtained. The contributions of the CoP and the counter-rotation mechanisms to control the CoM were calculated during steady-state walking, walking on LesSchuh, i.e. constraining mediolateral CoP shifts underneath the stance foot and walking on LesSchuh at 50% of normal step width, constraining both foot placement and ankle mechanisms (LesSchuh50%). A decreased magnitude of within-stride control by the CoP-mechanism was compensated for by an increased magnitude of within-stride control by the counter-rotation mechanism during LesSchuh50% compared to steady-state walking. This suggests that the counter-rotation mechanism is used to stabilize gait when needed. However, the mean contribution of the counter-rotation mechanism over strides did not increase during LesSchuh50% compared to steady-state walking. The CoP-mechanism was the main contributor to the total CoM acceleration. The use of the counter-rotation mechanism may be limited because angular accelerations ultimately need to be reversed and because of interference with other task constraints, such as head stabilization and preventing interference with the gait pattern.

Rethinking Margin of Stability: Incorporating Step-To-Step Regulation to Resolve the Paradox

ABSTRACTMaintaining frontal-plane stability is a major objective of human walking. Derived from inverted pendulum dynamics, the mediolateral Margin of Stability (MoSML) is frequently used to measure people’s frontal-plane stability on average. However, typical MoSML-based analyses deliver paradoxical interpretations of stability status. To address mediolateral stability using MoSML, we must first resolve this paradox. Here, we developed a novel framework that unifies the well-established inverted pendulum model with Goal-Equivalent Manifold (GEM)-based analyses to assess how humans regulate step-to-step balance dynamics to maintain mediolateral stability. We quantified the extent to which people corrected fluctuations in mediolateral center-of-mass state relative to a MoSML-defined candidate stability GEM in the inverted pendulum phase plane. Participants’ variability and step-to-step correction of tangent and perpendicular deviations from the candidate stability GEM demonstrate that regulation of balance dynamics involves more than simply trying to execute a constant-MoSML balance control strategy. Participants adapted these step-to-step corrections to mediolateral sensory and mechanical perturbations. How participants regulated mediolateral foot placement strongly predicted how they regulated center-of-mass state fluctuations, suggesting that regulation of center-of-mass state occurs as a biomechanical consequence of foot placement regulation. We introduce the Probability of Instability (PoI), a convenient statistic that accounts for step-to-step variance to properly predict instability likelihood on any given future step. Participants increased lateral PoI when destabilized, as expected. These lateral PoI indicated an increased risk of lateral instability, despite larger (i.e., more stable) average MoSML. PoI thereby explicitly predicts instability risk to decisively resolve the existing paradox that arises from conventional MoSML implementations.

Emergence of the London Millennium Bridge instability without synchronisation

The pedestrian-induced instability of the London Millennium Bridge is a widely used example of Kuramoto synchronisation. Yet, reviewing observational, experimental, and modelling evidence, we argue that increased coherence of pedestrians’ foot placement is a consequence of, not a cause of the instability. Instead, uncorrelated pedestrians produce positive feedback, through negative damping on average, that can initiate significant lateral bridge vibration over a wide range of natural frequencies. We present a simple general formula that quantifies this effect, and illustrate it through simulation of three mathematical models, including one with strong propensity for synchronisation. Despite subtle effects of gait strategies in determining precise instability thresholds, our results show that average negative damping is always the trigger. More broadly, we describe an alternative to Kuramoto theory for emergence of coherent oscillations in nature; collective contributions from incoherent agents need not cancel, but can provide positive feedback on average, leading to global limit-cycle motion.

Small Directional Treadmill Perturbations Induce Differential Gait Stability Adaptation

Introducing unexpected perturbations to challenge gait stability is an effective approach to investigate balance control strategies. Little is known about the extent to which people can respond to small perturbations during walking. This study aimed to determine how subjects adapted gait stability to multidirectional perturbations with small magnitudes applied on a stride-by-stride basis. Ten healthy young subjects walked on a treadmill that either briefly decelerated belt speed ("stick"), accelerated belt speed ("slip"), or shifted the platform medial-laterally at right leg mid-stance. We quantified gait stability adaptation in both anterior-posterior and medial-lateral directions using margin of stability and its components, base of support and extrapolated center of mass. Gait stability was disrupted upon initially experiencing the small perturbations as margin of stability decreased in the stick, slip, and medial shift perturbations and increased in the lateral shift perturbation. Gait stability metrics were generally disrupted more for perturbations in the coincident direction. Subjects employed both feedback and feedforward strategies in response to the small perturbations, but mostly used feedback strategies during adaptation. Subjects primarily used base of support (foot placement) control in the lateral shift perturbation and extrapolated center of mass control in the slip and medial shift perturbations. These findings provide new knowledge about the extent of gait stability adaptation to small magnitude perturbations applied on a stride-by-stride basis and reveal potential new approaches for balance training interventions to target foot placement and center of mass control.

Ankle muscles drive mediolateral center of pressure control to ensure stable steady state gait

During steady-state walking, mediolateral gait stability can be maintained by controlling the center of pressure (CoP). The CoP modulates the moment of the ground reaction force, which brakes and reverses movement of the center of mass (CoM) towards the lateral border of the base of support. In addition to foot placement, ankle moments serve to control the CoP. We hypothesized that, during steady-state walking, single stance ankle moments establish a CoP shift to correct for errors in foot placement. We expected ankle muscle activity to be associated with this complementary CoP shift. During treadmill walking, full-body kinematics, ground reaction forces and electromyography were recorded in thirty healthy participants. We found a negative relationship between preceding foot placement error and CoP displacement during single stance; steps that were too medial were compensated for by a lateral CoP shift and vice versa, steps that were too lateral were compensated for by a medial CoP shift. Peroneus longus, soleus and tibialis anterior activity correlated with these CoP shifts. As such, we identified an (active) ankle strategy during steady-state walking. As expected, absolute explained CoP variance by foot placement error decreased when walking with shoes constraining ankle moments. Yet, contrary to our expectations that ankle moment control would compensate for constrained foot placement, the absolute explained CoP variance by foot placement error did not increase when foot placement was constrained. We argue that this lack of compensation reflects the interdependent nature of ankle moment and foot placement control. We suggest that single stance ankle moments do not only compensate for preceding foot placement errors, but also assist control of the subsequent foot placement. Foot placement and ankle moment control are ‘caught’ in a circular relationship, in which constraints imposed on one will also influence the other.

Binocular vision and the control of foot placement during walking in natural terrain

Coordination between visual and motor processes is critical for the selection of stable footholds when walking in uneven terrains. While recent work (Matthis et al. in Curr Biol 8(28):1224–1233, 2018) demonstrates a tight link between gaze (visual) and gait (motor), it remains unclear which aspects of visual information play a role in this visuomotor control loop, and how the loss of this information affects that relationship. Here we examine the role of binocular information in the visuomotor control of walking over complex terrain. We recorded eye and body movements while normally-sighted participants walked over terrains of varying difficulty, with intact vision or with vision in one eye blurred to disrupt binocular vision. Gaze strategy was highly sensitive to the complexity of the terrain, with more fixations dedicated to foothold selection as the terrain became more difficult. The primary effect of increased sensory uncertainty due to disrupted binocular vision was a small bias in gaze towards closer footholds, indicating greater pressure on the visuomotor control process. Participants with binocular vision losses due to developmental disorders (i.e., amblyopia, strabismus), who have had the opportunity to develop alternative strategies, also biased their gaze towards closer footholds. Across all participants, we observed a relationship between an individual’s typical level of binocular visual function and the degree to which gaze is shifted toward the body. Thus the gaze–gait relationship is sensitive to the level of sensory uncertainty, and deficits in binocular visual function (whether transient or long-standing) have systematic effects on gaze strategy in complex terrains. We conclude that binocular vision provides useful information for locating footholds during locomotion. Furthermore, we have demonstrated that combined eye/body tracking in natural environments can be used to provide a more detailed understanding of the impact of a type of vision loss on the visuomotor control process of walking, a vital everyday task.

Learning from the physical consequences of our actions improves motor memory

Actions have consequences. Motor learning involves correcting actions that lead to movement errors and remembering these actions for future behavior. In most laboratory situations, movement errors have no physical consequences and simply indicate the progress of learning. Here we asked how experiencing a physical consequence when making a movement error affects motor learning. Two groups of participants adapted to a new, prism-induced mapping between visual input and motor output while performing a precision walking task. Importantly, one group experienced an unexpected slip perturbation when making foot-placement errors during adaptation. Because of our innate drive for safety, and the fact that balance is fundamental to movement, we hypothesized that this experience would enhance motor memory. Learning generalized to different walking tasks to a greater extent in the group who experienced the adverse physical consequence. This group also showed faster relearning one week later despite exposure to a competing mapping during initial learning—evidence of greater memory consolidation. The group differences in generalization and consolidation occurred even though they both experienced similar magnitude foot-placement errors and adapted at similar rates. Our results suggest the brain considers the potential physical consequences of movement error when learning and that balance-threatening consequences serve to enhance this process.