Caterpillar crawling over irregular terrain: anticipation and local sensing

Animal locomotion is produced by co-coordinated patterns of motor activity that are generally organized by central pattern generators and modified by sensory feedback. Animals with remote sensing can anticipate obstacles and make adjustments in their gait to accommodate them. It is largely unknown how animals that rely on touch might use such information to adjust their gait. One possibility is immediate (reflexive) change in motor activity. Elongated animals, however, might modulate movements by passing information from anterior to posterior segments. Using the caterpillar Manduca sexta we examined the movements of the most anterior abdominal prolegs as they approached an obstacle. The first pair of prolegs anticipated the obstacle by lifting more quickly in the earliest part of the swing phase: the caterpillar had information about the obstacle at proleg lift-off. Sometimes the prolegs corrected their trajectory mid-step. Removal of sensory hairs on the stepping leg did not affect the early anticipatory movements, but did change the distance at which the mid-step corrections occurred. We conclude that anterior sensory information can be passed backwards and used to modulate an ongoing crawl. The local sensory hairs on each body segment can then fine-tune movements of the prolegs as they approach an obstacle.     

Contributions of phase resetting and interlimb coordination to the adaptive control of hindlimb obstacle avoidance during locomotion in rats: a simulation study

Obstacle avoidance during locomotion is essential for safe, smooth locomotion. Physiological studies regarding muscle synergy have shown that the combination of a small number of basic patterns produces the large part of muscle activities during locomotion and the addition of another pattern explains muscle activities for obstacle avoidance. Furthermore, central pattern generators in the spinal cord are thought to manage the timing to produce such basic patterns. In the present study, we investigated sensory-motor coordination for obstacle avoidance by the hindlimbs of the rat using a neuromusculoskeletal model. We constructed the musculoskeletal part of the model based on empirical anatomical data of the rat and the nervous system model based on the aforementioned physiological findings of central pattern generators and muscle synergy. To verify the dynamic simulation by the constructed model, we compared the simulation results with kinematic and electromyographic data measured during actual locomotion in rats. In addition, we incorporated sensory regulation models based on physiological evidence of phase resetting and interlimb coordination and examined their functional roles in stepping over an obstacle during locomotion. Our results show that the phase regulation based on interlimb coordination contributes to stepping over a higher obstacle and that based on phase resetting contributes to quick recovery after stepping over the obstacle. These results suggest the importance of sensory regulation in generating successful obstacle avoidance during locomotion.     

A self-organizing model of walking patterns of insects

Insects generate walking patterns which depend upon external conditions. For example, when an insect is exposed to an additional load parallel to the direction in which it is walking, the walking pattern changes according to the magnitude of the load. Furthermore, even after some of its legs have been amputated, an insect will produce walking patterns with its remaining legs. These adaptations in insect walking could not previously be explained by a mathematical model, since the mathemati cal models were based upon the hypothesis that the relationship between walking velocity and walking patterns is fixed under all conditions. We have produced a mathematical model which describes self-organizing insect walking patterns in real-time by using feedback information regarding muscle load (Kimura et al. 1993). As part of this model, we introduced a new rule to coordinate leg movement, in which the information is circulated to optimize the efficiency of the energy transduction of each effector orga n. We describe this mechanism as ‘the least dissatisfaction for the greatest number of elements’. In this paper, we introduce the following aspects of this model, which reflect adaptability to changing circumstances: (1) after one leg is exposed to a transient perturbation, the walking pattern recovers swiftly; (2) when the external load parallel to the walking direction is continuously increased or decreased, the pattern transition point is shifted according to the magnitude of the load increme nt or decrement. This model generates a walking pattern which optimizes energy consumption at a given walking velocity even under these conditions; and (3) when some of the legs are amputated, the model generates walking patterns which are consistent with experimental results. We also discuss the ability of a hierarchical self-organizing model to describe a swift and flexible information processing system. Received: 8 February 1993/Accepted in revised form: 12 November 1993     

Age-related and obstacle height-related differences in movements while stepping over obstacles

Background

This study aims to examine age-related and obstacle height-related differences in movements while stepping over obstacles.

Methods

The participants included 16 elderly and nine young women. Obstacles that were either 5 or 20 cm high were positioned at the center of a 4-m walking path. The participants were instructed to walk along the path as quickly as possible. The participants’ movements were analyzed using a three-dimensional motion analysis system that recorded their movements as they walked and stepped over the obstacles.

Results and conclusions

Seven joint angles and the distances between the ground and six markers were examined in the initial contact and swing instants of the leading and trailing limbs. In the initial contact instant, the elderly women prepared for stepping with a lower toe height than the young women when stepping over the 20-cm obstacle. Trunk rotation was greater in the young women than in the elderly women. In the swing instant, the elderly women showed greater ankle dorsiflexion and hip adduction angles for the leading limb when stepping over the 20-cm obstacle. They moved the trailing limb with increased ankle dorsiflexion, knee flexion, hip flexion, and foot inversion to ensure that they did not touch the obstacle as they stepped over it. These movement patterns are characteristic of elderly individuals who cannot easily lift their lower limbs because of decreased lower-limb strength.     

Infant stepping: a window to the behaviour of the human pattern generator for walking

The aim of this paper is to provide evidence, both published and new, to support the notion that human infants are particularly good subjects for the study of the pattern generator for walking. We and others have shown that stepping can be initiated by sensory input from the legs or by general heightened excitability of the infant. New results are presented here to suggest that weight support through the feet and rapid extension of the legs are important proprioceptive inputs to initiate stepping. Our previous work has shown that infants can step at many different speeds when supported on a treadmill. The step cycle duration shortens as the speed increases, with the changes coming largely from the stance phase, just as in most other terrestrial animals. Moreover, we have shown that infants will step in all directions. Regardless of the direction of stepping, the step cycle changes in the same way with walking speed, suggesting the circuitry that controls different directions of walking share common elements. We have also shown that infant stepping is highly organized. Sensory inputs, whether proprioceptive or touch, are gated in a functional way so that only important sensory inputs generate a response. For example, touch to the lateral surface of the foot elicits a response only in sideways walking, and only in the leading limb. New data is presented here to show that the pattern generators from each limb can operate somewhat independently. On a split-belt treadmill with the 2 belts running at different speeds or in different directions, the legs showed considerable independence in behaviour. Yet, the pattern generators on each side interact to ensure that swing phase does not occur at the same time. These studies have provided insight into the organization of the pattern generator for walking in humans. It will be interesting in the future to study how maturation of the descending tracts changes walking behaviour to allow independent bipedal walking.     

Locomotor Adaptation versus Perceptual Adaptation when Stepping Over an Obstacle with a Height Illusion

Background

During locomotion, vision is used to perceive environmental obstacles that could potentially threaten stability; locomotor action is then modified to avoid these obstacles. Various factors such as lighting and texture can make these environmental obstacles appear larger or smaller than their actual size. It is unclear if gait is adapted based on the actual or perceived height of these environmental obstacles. The purposes of this study were to determine if visually guided action is scaled to visual perception, and to determine if task experience influenced how action is scaled to perception.

Methodology/Principal Findings

Participants judged the height of two obstacles before and after stepping over each of them 50 times. An illusion made obstacle one appear larger than obstacle two, even though they were identical in size. The influence of task experience was examined by comparing the perception-action relationship during the first five obstacle crossings (1–5) with the last five obstacle crossings (46–50). In the first set of trials, obstacle one was perceived to be 2.0 cm larger than obstacle two and subjects stepped 2.7 cm higher over obstacle one. After walking over the obstacle 50 times, the toe elevation was not different between obstacles, but obstacle one was still perceived as 2.4 cm larger.

Conclusions/Significance

There was evidence of locomotor adaptation, but no evidence of perceptual adaptation with experience. These findings add to research that demonstrates that while the motor system can be influenced by perception, it can also operate independent of perception.     

Experimental modification of stepping course in spontaneously initiated locomotor behavior in the crayfish Procambarus clarkii Girard

The stepping course in spontaneously initiated walking of crayfish was quantitatively analyzed using a spherical treadmill system. In complete darkness, some animals stepped either forward or backward at random whereas others showed individually a consistent tendency of stepping in a specific direction although no external sensory cue was provided. The tendency was statistically significant and invariable for at least 6-8 h. When a light stimulus was present in front of the animal, the stepping course tended to be backward or curved forward to avoid the stimulus. Either in complete darkness or in the presence of a light stimulus, the animal's tendency to step in a specific direction could be modified experimentally by applying electrical stimulation to a part of the animal body upon stepping in the preferred direction. The newly acquired tendency of stepping direction could be retained for 6 h and modified again by a similar procedure of electric stimulation. Both before and after modification of the stepping course tendency, animals seldom changed their stepping direction once the walking was initiated. These findings suggest that the stepping course in spontaneously initiated walking is significantly affected by animal's previous experience and could be predetermined at the onset of walking.     

Interactions between cognitive and sensory load while planning and controlling complex gait adaptations in Parkinson’s disease

Background

Recent research has argued that removal of relevant sensory information during the planning and control of simple, self-paced walking can result in increased demand on central processing resources in Parkinson’s disease (PD). However, little is known about more complex gait tasks that require planning of gait adaptations to cross over an obstacle in PD.

Methods

In order to understand the interaction between availability of visual information relevant for self-motion and cognitive load, the current study evaluated PD participants and healthy controls while walking toward and stepping over an obstacle in three visual feedback conditions: (i) no visual restrictions; (ii) vision of the obstacle and their lower limbs while in complete darkness; (iii) vision of the obstacle only while in complete darkness; as well as two conditions including a cognitive load (with a dual task versus without a dual task). Each walk trial was divided into an early and late phase to examine changes associated with planning of step adjustments when approaching the obstacle.

Results

Interactions between visual feedback and dual task conditions during the obstacle approach were not significant. Patients with PD had greater deceleration and step time variability in the late phase of the obstacle approach phase while walking in both dark conditions compared to control participants. Additionally, participants with PD had a greater number of obstacle contacts when vision of their lower limbs was not available specifically during the dual task condition. Dual task performance was worse in PD compared to healthy control participants, but notably only while walking in the dark regardless of visual feedback.

Conclusions

These results suggest that reducing visual feedback while approaching an obstacle shifts processing to somatosensory feedback to guide movement which imposes a greater demand on planning resources. These results are key to fully understanding why trips and falls occur in those with PD.

     

Obstacle avoidance in Down syndrome

IntroductionThe ability to avoid obstacles requires to represent the properties of the obstacle, represent the location of the obstacle relative to the body and update these representations as the body moves. Individuals with Down syndrome (DS) often have trouble avoiding obstacles, leading to increased frequency of trips and falling. The aim of the present study was to deeply analyze obstacle avoidance strategies in normally developed young adults (N) and in young adults with DS, at different levels of obstacle heights, with particular attention to the strategies used for clearing the obstacle and to how the walking pattern was modified by obstacle perception.Methods10 DS and 16 age-matched N walked along a walkway in three conditions: plain walking, walking with obstacle at ground level, walking with obstacle at 10% of the subject’s height. Spatiotemporal parameters were analyzed.ResultsThere was evidence for a different avoidance strategy in DS, and for a difficulty in regulating gait parameters when challenged with a complex situation as the presence of an obstacle. This may lead to an increased risk of fall. The results in addition suggested a lack in anticipatory movement adjustments in DS and provided further evidence of the presence of difficulties in perceptual–motor coupling in DS.     

Observing a Movement Correction during Walking Affects Evoked Responses but Not Unperturbed Walking

Seeing an action activates neurons in the premotor, motor, and somatosensory cortex. Since a significant fraction of these pyramidal neurons project to the spinal motor circuits, a central question is why we do not automatically perform the actions that we see. Indeed, seeing an action increases both cortical and spinal excitability of consistent motor patterns that correspond to the observed ones. Thus, it is believed that such imitative motor patterns are either suppressed or remain at a sub-threshold level. This would predict, however, that seeing someone make a corrective movement while one is actively involved in the same action should either suppress evoked responses or suppress or modulate the action itself. Here we tested this prediction, and found that seeing someone occasionally stepping over an obstacle while walking on a treadmill did not affect the normal walking pattern at all. However, cutaneously evoked reflexes in the anterior tibial and soleus muscles were modulated as if the subject was stepping over an obstacle. This result thus indicates that spinal activation was not suppressed and was neither at sub-threshold motor resonance. Rather, the spinal modulation from observed stepping reflects an adaptive mechanism for regulating predictive control mechanisms. We conclude that spinal excitability during action observation is not an adverse side-effect of action understanding but reflects adaptive and predictive motor control.     

Energy efficient walking with central pattern generators: from passive dynamic walking to biologically inspired control

Like human walking, passive dynamic walking—i.e. walking down a slope with no actuation except gravity—is energy efficient by exploiting the natural dynamics. In the animal world, neural oscillators termed central pattern generators (CPGs) provide the basic rhythm for muscular activity in locomotion. We present a CPG model, which automatically tunes into the resonance frequency of the passive dynamics of a bipedal walker, i.e. the CPG model exhibits resonance tuning behavior. Each leg is coupled to its own CPG, controlling the hip moment of force. Resonance tuning above the endogenous frequency of the CPG—i.e. the CPG’s eigenfrequency—is achieved by feedback of both limb angles to their corresponding CPG, while integration of the limb angles provides resonance tuning at and below the endogenous frequency of the CPG. Feedback of the angular velocity of both limbs to their corresponding CPG compensates for the time delay in the loop coupling each limb to its CPG. The resonance tuning behavior of the CPG model allows the gait velocity to be controlled by a single parameter, while retaining the energy efficiency of passive dynamic walking.     

From swimming to walking: a single basic network for two different behaviors

 In this paper we consider the hypothesis that the spinal locomotor network controlling trunk movements has remained essentially unchanged during the evolutionary transition from aquatic to terrestrial locomotion. The wider repertoire of axial motor patterns expressed by amphibians would then be explained by the influence from separate limb pattern generators, added during this evolution. This study is based on EMG data recorded in vivo from epaxial musculature in the newt Pleurodeles waltl during unrestrained swimming and walking, and on a simplified model of the lamprey spinal pattern generator for swimming. Using computer simulations, we have examined the output generated by the lamprey model network for different input drives. Two distinct inputs were identified which reproduced the main features of the swimming and walking motor patterns in the newt. The swimming pattern is generated when the network receives tonic excitation with local intensity gradients near the neck and girdle regions. To produce the walking pattern, the network must receive (in addition to a tonic excitation at the girdles) a phasic drive which is out of phase in the neck and tail regions in relation to the middle part of the body. To fit the symmetry of the walking pattern, however, the intersegmental connectivity of the network had to be modified by reversing the direction of the crossed inhibitory pathways in the rostral part of the spinal cord. This study suggests that the input drive required for the generation of the distinct walking pattern could, at least partly, be attributed to mechanosensory feedback received by the network directly from the intraspinal stretch-receptor system. Indeed, the input drive required resembles the pattern of activity of stretch receptors sensing the lateral bending of the trunk, as expressed during walking in urodeles. Moreover, our results indicate that a nonuniform distribution of these stretch receptors along the trunk can explain the discontinuities exhibited in the swimming pattern of the newt. Thus, separate limb pattern generators can influence the original network controlling axial movements not only through a direct coupling at the central level but also via a mechanical coupling between trunk and limbs, which in turn influences the sensory signals sent back to the network. Taken together, our findings support the hypothesis of a phylogenetic conservatism of the spinal locomotor networks generating axial motor patterns from agnathans to amphibians. Received: 12 October 2001 / Accepted in revised form: 16 May 2002 Correspondence to: T. Bem (e-mail: tiaza.bem@ibib.waw.pl)     

Gait Transitions in Human Infants: Coping with Extremes of Treadmill Speed

Spinal pattern generators in quadrupedal animals can coordinate different forms of locomotion, like trotting or galloping, by altering coordination between the limbs (interlimb coordination). In the human system, infants have been used to study the subcortical control of gait, since the cerebral cortex and corticospinal tract are immature early in life. Like other animals, human infants can modify interlimb coordination to jump or step. Do human infants possess functional neuronal circuitry necessary to modify coordination within a limb (intralimb coordination) in order to generate distinct forms of alternating bipedal gait, such as walking and running? We monitored twenty-eight infants (7–12 months) stepping on a treadmill at speeds ranging between 0.06–2.36 m/s, and seventeen adults (22–47 years) walking or running at speeds spanning the walk-to-run transition. Six of the adults were tested with body weight support to mimic the conditions of infant stepping. We found that infants could accommodate a wide range of speeds by altering stride length and frequency, similar to adults. Moreover, as the treadmill speed increased, we observed periods of flight during which neither foot was in ground contact in infants and in adults. However, while adults modified other aspects of intralimb coordination and the mechanics of progression to transition to a running gait, infants did not make comparable changes. The lack of evidence for distinct walking and running patterns in infants suggests that the expression of different functional, alternating gait patterns in humans may require neuromuscular maturation and a period of learning post-independent walking.     

Hermit crabs perceive the extent of their virtual bodies

A flexible body image is required by animals if they are to adapt to body changes and move effectively within a structurally complex environment. Here, we show that terrestrial hermit crabs, Coenobita rugosus, which frequently change shells, can modify walking behaviour, dependent on the shape of the shell. Hermit crabs walked along a corridor that had alternating left and right corners; if it was narrow at the corner, crabs rotated their bodies to avoid the wall, indicating an awareness of environmental obstacles. This rotation increased when a plastic plate was attached to the shell. We suggest that the shell, when extended by the plate, becomes assimilated to the hermit crab's own body. While there are cases of a tool being assimilated with the body, our result is the first example of the habitat where an animal lives and/or carries being part of a virtual body.     

Simulated control of unilateral,anticipatory locomotor adjustments during obstructed gait

Anticipatory adjustments of our locomotor patterns are necessary in order to negotiate our uneven daily environments. Recent work (McFadyen and Winter 1991) has shown the re-organization of lower limb mechanics for obstacle avoidance during level walking. The present work describes a model which sets the ground work for predicting how such re-organized motor patterns might be generated from stereotypic unobstructed patterns. Pattern-generating algorithms use an estimation of future contacts with obstacles to create weighting functions that modify joint angle trajectories towards new patterns capable of clearing the obstacle. Feedforward/feedback control is then used to generate the necessary joint torques. The results show that model parameters can be found to generate not only kinematic but also energetic patterns for obstacle clearance that mimic experimental results. The validity of the model with respect to human locomotor control is discussed.     

The functional sense of central oscillations in walking

 Rhythmic motor output is generally assumed to be produced by central pattern generators or, more specific, central oscillators, the rhythmic output of which can be entrained and modulated by sensory input and descending control. In the case of locomotor systems, the output of the central system, i.e., the output obtained after deafferentation of sensory feedback, shows many of the temporal characteristics of real movements. Therefore the term fictive locomotion has been coined. This article concentrates on a specific locomotor behavior, namely walking; in particular walking in invertebrates. In contrast to the traditional view, an alternative hypothesis is formulated to interpret the functional sense of these central oscillations which have been found in many cases. It is argued that the basic function of the underlying circuit is to avoid cocontraction of antagonistic muscles. Such a system operates best with an inherent period just above the maximum period observed in real walking. The circuit discussed in this article (Fig. 2) shows several properties in common with results described as “fictive walking”. It furthermore could explain a number of properties observed in animals walking in different situations. According to this hypothesis, the oscillations found after deafferentation are side effects occurring in specific artificial situations. If, however, a parameter called central excitation is large enough, the system can act as a central oscillator that overrides the sensory input completely. Received: 18 May 2001 / Accepted in revised form: 20 November 2001     

A mathematical modeling study of inter-segmental coordination during stick insect walking

The biomechanical conditions for walking in the stick insect require a modeling approach that is based on the control of pairs of antagonistic motoneuron (MN) pools for each leg joint by independent central pattern generators (CPGs). Each CPG controls a pair of antagonistic MN pools. Furthermore, specific sensory feedback signals play an important role in the control of single leg movement and in the generation of inter-leg coordination or the interplay between both tasks. Currently, however, no mathematical model exists that provides a theoretical approach to understanding the generation of coordinated locomotion in such a multi-legged locomotor system. In the present study, I created such a theoretical model for the stick insect walking system, which describes the MN activity of a single forward stepping middle leg and helps to explain the neuronal mechanisms underlying coordinating information transfer between ipsilateral legs. In this model, CPGs that belong to the same leg, as well as those belonging to different legs, are connected by specific sensory feedback pathways that convey information about movements and forces generated during locomotion. The model emphasizes the importance of sensory feedback, which is used by the central nervous system to enhance weak excitatory and inhibitory synaptic connections from front to rear between the three thorax-coxa-joint CPGs. Thereby the sensory feedback activates caudal pattern generation networks and helps to coordinate leg movements by generating in-phase and out-of-phase thoracic MN activity.     

Electromyographic characterization of walking behavior initiated spontaneously in crayfish

Crayfish initiate walking behavior not only reflexively in response to external stimuli but also spontaneously in the absence of any specific stimulus. In order to analyze the initiation mechanism underlying these different types of walking, we made simultaneous electromyographic (EMG) recordings from thoracic legs when animals initiated walking, either reflexively or spontaneously, and video recorded their movements synchronously with the EMG recording. Two different stimuli, mechanical and chemical, were used to reflexively induce walking. A non-rhythmic, sustained activation of leg muscles was found to precede the behavioral initiation of either type of walking. The duration of this non-rhythmic muscle activation was significantly longer in the spontaneously initiated walking than in the mechanical stimulus-evoked walking, although no difference was observed between the spontaneous and chemical stimulus-evoked walking. EMG recordings from all eight legs revealed that their non-rhythmic muscle activation occurred almost simultaneously prior to initiation of rhythmical stepping movements. When an animal was suspended without a leg substratum, the timing of muscle activation was more variable among the legs than in the free condition on the substratum. When the circumesophageal commissures were both severed to eliminate signals descending from the brain to the thoracic ganglia, the bilaterally coordinated rhythmic burst activity was not observed in the walking legs. These findings suggest that the spontaneous initiation of walking behavior requires sensory feedback signals from leg proprioceptors, subserved by a different descending activation mechanism from that for stimulus-driven initiation of walking.     

Parameter optimization model of learning in stepping motion

In this study we combine the representation of motion by a finite number of hardwired functions with parameter optimization to model learning during a stepping motion. Representation of experimental kinematic data by a finite number of predetermined functions and undetermined coefficients was analyzed. Least squares approximation was used to represent experimental data of stepping motions over obstacles of different heights. Functional relationships between coefficients and obstacles heights were also obtained. Learning of stepping over an obstacle was then formulated as a finite dimensional optimization problem. The pattern of foot path, and joint angles trajectories obtained by this learning model, were then compared to the experimental data. The results of the data fitting analysis and of the optimization process as a model for motion learning, indicate that motion can be adequately represented by a set of hardwired functions, and a finite number of task dependent coefficients.