An official website of the United States government
Key pointsVision plays a crucial role in guiding locomotion in complex environments, but the coordination between gaze and stride is not well understood.The coordination of gaze shifts, fixations, constant gaze and slow gaze with strides in cats walking on different surfaces were examined.It was found that gaze behaviours are coordinated with strides even when walking on a flat surface in the complete darkness, occurring in a sequential order during different phases of the stride.During walking on complex surfaces, gaze behaviours are typically more tightly coordinated with strides, particularly at faster speeds, only slightly shifting in phase.These findings indicate that the coordination of gaze behaviours with strides is not vision‐driven, but is a part of the whole body locomotion synergy; the visual environment and locomotor task modulate it. The results may be relevant to developing diagnostic tools and rehabilitation approaches for patients with locomotor deficits. AbstractVision plays a crucial role in guiding locomotion in complex environments. However, the coordination between the gaze and stride is not well understood. We investigated this coordination in cats walking on a flat surface in darkness or light, along a horizontal ladder and on a pathway with small stones. We recorded vertical and horizontal eye movements and 3‐D head movement, and calculated where gaze intersected the walkway. The coordination of gaze shifts away from the animal, gaze shifts toward, fixations, constant gaze, and slow gaze with strides was investigated. We found that even during walking on the flat surface in the darkness, all gaze behaviours were coordinated with strides. Gaze shifts and slow gaze toward started in the beginning of each forelimb's swing and ended in its second half. Fixations peaked throughout the beginning and middle of swing. Gaze shifts away began throughout the second half of swing of each forelimb and ended when both forelimbs were in stance. Constant gaze and slow gaze away occurred in the beginning of stance. However, not every behaviour occurred during every stride. Light had a small effect. The ladder and stones typically increased the coordination and caused gaze behaviours to occur 3% earlier in the cycle. At faster speeds, the coordination was often tighter and some gaze behaviours occurred 2–16% later in the cycle. The findings indicate that the coordination of gaze with strides is not vision‐driven, but is a part of the whole body locomotion synergy; the visual environment and locomotor task modulate it.
more »
« less
When cats need to see to step accurately?
Locomotion on complex terrains often requires vision. However, how vision serves locomotion is not well understood. Here, we asked when visual information necessary for accurate stepping is collected and how its acquisition relates to the step cycle. In cats of both sexes, we showed that a brief (200–400 ms) interruption of visual input can rapidly influence cat’s walking along a horizontal ladder. Depending on the phase within the step cycle, a 200 ms period of darkness could be tolerated fully without any changes to the strides or could lead to minor increases of stride duration. The effects of 300–400 ms of visual input denial, which typically prolonged stances and/or swings, also depended on the phase of the darkness onset. The increase of the duration of strides was always shorter than the duration of darkness. We conclude that visual information for planning a swing is collected starting from the middle of the preceding stance until the beginning of the current swing. For a stance (and/or a swing of the other paw), visual information is collected starting from the end of the previous stance and until the middle of the current stance. Acquisition of visual information during these windows is not uniform but depends on the phase of the step cycle. Notably, both the extension of these windows and their non-homogeneity are closely related to the pattern of gaze behaviour in cats, described previously. This new knowledge will help to guide research and understanding of neuronal mechanisms of visuomotor integration and modulation of visual function by strides during locomotion.
more »
« less
- Award ID(s):
- 1912557
- PAR ID:
- 10309470
- Date Published:
- Journal Name:
- The Journal of Physiology
- ISSN:
- 0022-3751
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
The activity of motor cortex is necessary for accurate stepping on a complex terrain. How this activity is generated remains unclear. The goal of this study was to clarify the contribution of signals from the ventrolateral thalamus (VL) to formation of locomotion-related activity of motor cortex during vision-independent and vision-dependent locomotion. In two cats, we recorded the activity of neurons in layer V of motor cortex as cats walked on a flat surface and a horizontal ladder. We reversibly inactivated ~10% of the VL unilaterally with the glutamatergic transmission antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and analyzed how this affected the activity of motor cortex neurons. We examined neuronal subpopulations with somatosensory receptive fields on different segments of the forelimb and pyramidal tract projecting neurons (PTNs). We found that the VL contribution to the locomotion-related activity of motor cortex is very powerful and has both excitatory and inhibitory components. The magnitudes of both the excitatory and inhibitory contributions fluctuate over the step cycle and depend on locomotion task. On a flat surface, the VL contributes more excitation to the shoulder- and elbow-related neurons than the wrist/paw-related cells. The VL excites the shoulder-related group the most during the transition from stance to swing phase, while most intensively exciting the elbow-related group during the transition from swing to stance. The VL contributes more excitation for the fast- than slow-conducting PTNs. Upon transition to vision-dependent locomotion on the ladder, the VL contribution increases more for the wrist/paw-related neurons and slow-conducting PTNs. NEW & NOTEWORTHY How the activity of motor cortex is generated and the roles that different inputs to motor cortex play in formation of response properties of motor cortex neurons during movements remain unclear. This is the first study to characterize the contribution of the input from the ventrolateral thalamus (VL), the main subcortical input to motor cortex, to the activity of motor cortex neurons during vision-independent and vision-dependent locomotion.more » « less
-
Abstract Existing models of human walking use low-level reflexes or neural oscillators to generate movement. While appropriate to generate the stable, rhythmic movement patterns of steady-state walking, these models lack the ability to change their movement patterns or spontaneously generate new movements in the specific, goal-directed way characteristic of voluntary movements. Here we present a neuromuscular model of human locomotion that bridges this gap and combines the ability to execute goal directed movements with the generation of stable, rhythmic movement patterns that are required for robust locomotion. The model represents goals for voluntary movements of the swing leg on the task level of swing leg joint kinematics. Smooth movements plans towards the goal configuration are generated on the task level and transformed into descending motor commands that execute the planned movements, using internal models. The movement goals and plans are updated in real time based on sensory feedback and task constraints. On the spinal level, the descending commands during the swing phase are integrated with a generic stretch reflex for each muscle. Stance leg control solely relies on dedicated spinal reflex pathways. Spinal reflexes stimulate Hill-type muscles that actuate a biomechanical model with eight internal joints and six free-body degrees of freedom. The model is able to generate voluntary, goal-directed reaching movements with the swing leg and combine multiple movements in a rhythmic sequence. During walking, the swing leg is moved in a goal-directed manner to a target that is updated in real-time based on sensory feedback to maintain upright balance, while the stance leg is stabilized by low-level reflexes and a behavioral organization switching between swing and stance control for each leg. With this combination of reflex-based stance leg and voluntary, goal-directed control of the swing leg, the model controller generates rhythmic, stable walking patterns in which the swing leg movement can be flexibly updated in real-time to step over or around obstacles.more » « less
-
Abstract Navigating complex terrains requires dynamic interactions between the substrate, musculoskeletal, and sensorimotor systems. Current perturbation studies have mostly used visible terrain height perturbations, which do not allow us to distinguish among the neuromechanical contributions of feedforward control, feedback-mediated, and mechanical perturbation responses. Here, we use treadmill-belt speed perturbations to induce a targeted perturbation to foot speed only, and without terrain-induced changes in joint posture and leg loading at stance onset. Based on previous studies suggesting a proximo-distal gradient in neuromechanical control, we hypothesized that distal joints would exhibit larger changes in joint kinematics, compared to proximal joints. Additionally, we expected birds to use feedforward strategies to increase the intrinsic stability of gait. To test these hypotheses, seven adult guinea fowl were video recorded while walking on a motorized treadmill, during both steady and perturbed trials. Perturbations consisted of repeated exposures to a deceleration and acceleration of the treadmill-belt speed. Surprisingly, we found that joint angular trajectories and center of mass fluctuations remain very similar, despite substantial perturbation of foot velocity by the treadmill belt. Hip joint angular trajectories exhibit the largest changes, with the birds adopting a slightly more flexed position across all perturbed strides. Additionally, we observed increased stride duration across all strides, consistent with feedforward changes in the control strategy. The speed perturbations mainly influenced the timing of stance and swing, with the largest kinematic changes in the strides directly following a deceleration. Our findings do not support the general hypothesis of a proximo-distal gradient in joint control, as distal joint kinematics remain largely unchanged. Instead, we find that leg angular trajectory and the timing of stance and swing are most sensitive to this specific perturbation, and leg length actuation remains largely unchanged. Our results are consistent with modular task-level control of leg length and leg angle actuation, with different neuromechanical control and perturbation sensitivity in each actuation mode. Distal joints appear to be sensitive to changes in vertical loading but not foot fore-aft velocity. Future directions should include in vivo studies of muscle activation and force–length dynamics to provide more direct evidence of the sensorimotor control strategies for stability in response to belt-speed perturbations.more » « less
-
Many control methods have been proposed for powered prosthetic legs, ranging from finite state machines that switch between discrete phases of gait to unified controllers that have a continuous sense of phase. In particular, recent work has shown that a mechanical phase variable can parameterize the entire gait cycle for controlling a prosthetic leg during steady rhythmic locomotion. However, the unified approach does not provide voluntary control over non-rhythmic motions like stepping forward and back. In this paper we present a phasing algorithm that uses the amputee’s hip angle to control both rhythmic and non-rhythmic motion through two modes: 1) a piecewise (PW) function that provides users voluntary control over stance and swing in a piecewise manner, and 2) a unified function that continuously synchronizes the motion of the prosthetic leg with the amputee user at different walking speeds. The two phase variable approaches are compared in experiments with a powered knee-ankle prosthesis used by an above-knee amputee subject.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1113/JP282255
