Coupling of upper and lower limb pattern generators during human crawling at different arm/leg speed combinations

A crawling paradigm was performed by healthy adults to examine inter-limb coupling patterns and to understand how central pattern generators (CPGs) for the upper and lower limbs are coordinated. Ten participants performed hands-and-feet crawling on two separate treadmills, one for the upper limbs and another one for the lower limbs, the speed of each of them being changed independently. A 1:1 frequency relationship was often maintained even when the treadmill speed was not matched between the upper and lower limbs. However, relative stance durations in the upper limbs were only affected by changes of the upper limb treadmill speed, suggesting that although absolute times are adjusted, the relative proportions of stances and swing do not adapt to changes in lower limb treadmill speeds. With large differences between treadmill speeds, changes in upper and lower limb coupling ratio tended to occur when the upper limbs stepped at slower speeds than the lower limbs, but more rarely the other way around. These findings are in sharp contrast with those in the cat, where forelimbs always follow the rhythm of the faster moving hindlimbs. However, the fact that an integer frequency ratio is often maintained between the upper and lower limbs supports evidence of coupled CPG control. We speculate that the preference for the upper limb to decrease step frequency at lower speeds in humans may be due to weaker ascending propriospinal connections and/or a larger influence of cortical control on the upper limbs which allows for an overriding of spinal CPG control

Foot Placement Characteristics and Plantar Pressure Distribution Patterns during Stepping on Ground in Neonates

Stepping on ground can be evoked in human neonates, though it is rather irregular and stereotyped heel-to-toe roll-over pattern is lacking. Such investigations can provide insights into the role of contact- or load-related proprioceptive feedback during early development of locomotion. However, the detailed characteristics of foot placements and their association with motor patterns are still incompletely documented. We elicited stepping in 33 neonates supported on a table. Unilateral limb kinematics, bilateral plantar pressure distribution and EMG activity from up to 11 ipsilateral leg muscles were recorded. Foot placement characteristics in neonates showed a wide variation. In ~25% of steps, the swinging foot stepped onto the contralateral foot due to generally small step width. In the remaining steps with separate foot placements, the stance phase could start with forefoot (28%), midfoot (47%), or heel (25%) touchdowns. Despite forefoot or heel initial contacts, the kinematic and loading patterns markedly differed relatively to toe-walking or adult-like two-peaked vertical force profile. Furthermore, while the general stepping parameters (cycle duration, step length, range of motion of proximal joints) were similar, the initial foot contact was consistently associated with specific center-of-pressure excursion, range of motion in the ankle joint, and the center-of-activity of extensor muscles (being shifted by ~5% of cycle toward the end of stance in the “heel” relative to “forefoot” condition). In sum, we found a variety of footfall patterns in conjunction with associated changes in motor patterns. These findings suggest the potential contribution of load-related proprioceptive feedback and/or the expression of variations in the locomotor program already during early manifestations of stepping on ground in human babies

Can modular strategies simplify neural control of multidirectional human locomotion?

Each human lower-limb contains over 50 muscles that are coordinated during locomotion. It has been hypothesized that the nervous system simplifies muscle control through modularity, using neural patterns to activate muscles in groups called synergies. Here we investigate how simple modular controllers based on invariant neural primitives (synergies or patterns) might generate muscle activity observed during multidirectional locomotion. We extracted neural primitives from unilateral electromyographic recordings of 25 lower-limb muscles during five locomotor tasks, walking forwards, backwards, leftwards, rightwards and stepping in place. A subset of subjects also performed five variations of forward (unidirectional) walking: self-selected cadence, fast cadence, slow cadence, tiptoe and uphill (20% incline). We assessed the results in the context of dimensionality reduction, defined here as the number of neural signals needing to be controlled. For individual tasks we found that modular architectures could theoretically reduce dimensionality compared to independent muscle control, but we also observed trade-offs for each strategy. Specifically, we found that modular strategies relying on neural primitives shared across different tasks were limited in their ability to account for muscle activations during multi- and uni-directional locomotion. The utility of shared primitives may thus depend on if they can be adapted for specific task demands, for instance, by means of sensory feedback or by being embedded within a more complex sensorimotor controller. Our findings indicate the need for more sophisticated formulations of modular control or alternative motor control hypotheses in order to understand muscle coordination during locomotion

Spinal motor outputs during step-to-step transitions of diverse human gaits

Aspects of human motor control can be inferred from the coordination of muscles during movement. For instance, by combining multimuscle electromyographic (EMG) recordings with human neuroanatomy, it is possible to estimate alpha-motoneuron (MN) pool activations along the spinal cord. It has previously been shown that the spinal motor output fluctuates with the body's center-of-mass motion, with bursts of activity around foot-strike and foot lift-off during walking. However, it is not known whether these MN bursts are generalizable to other ambulation tasks, nor is it clear if the spatial locus of the activity (along the rostrocaudal axis of the spinal cord) is fixed or variable. Here we sought to address these questions by investigating the spatiotemporal characteristics of the spinal motor output during various tasks: walking forward, backward, tiptoe and uphill. We reconstructed spinal maps from 26 leg muscle EMGs, including some intrinsic foot muscles. We discovered that the various walking tasks shared qualitative similarities in their temporal spinal activation profiles, exhibiting peaks around foot-strike and foot-lift. However, we also observed differences in the segmental level and intensity of spinal activations, particularly following foot-strike. For example, forward level-ground walking exhibited a mean motor output roughly 2 times lower than the other gaits. Finally, we found that the reconstruction of the spinal motor output from multimuscle EMG recordings was relatively insensitive to the subset of muscles analyzed. In summary, our results suggested temporal similarities, but spatial differences in the segmental spinal motor outputs during the step-to-step transitions of disparate walking behaviors

Coordination of intrinsic and extrinsic foot muscles during walking

The human foot undergoes complex deformations during walking due to passive tissues and active muscles. However, based on prior recordings it is unclear if muscles that contribute to flexion/extension of the metatarsophalangeal (MTP) joints are activated synchronously to modulate joint impedance, or sequentially to perform distinct biomechanical functions. We investigated the coordination of MTP flexors and extensors with respect to each other, and to other ankle-foot muscles

Gravity in the Brain as a Reference for Space and Time Perception

Moving and interacting with the environment require a reference for orientation and a scale for calibration in space and time. There is a wide variety of environmental clues and calibrated frames at different locales, but the reference of gravity is ubiquitous on Earth. The pull of gravity on static objects provides a plummet which, together with the horizontal plane, defines a three-dimensional Cartesian frame for visual images. On the other hand, the gravitational acceleration of falling objects can provide a time-stamp on events, because the motion duration of an object accelerated by gravity over a given path is fixed. Indeed, since ancient times, man has been using plumb bobs for spatial surveying, and water clocks or pendulum clocks for time keeping. Here we review behavioral evidence in favor of the hypothesis that the brain is endowed with mechanisms that exploit the presence of gravity to estimate the spatial orientation and the passage of time. Several visual and non-visual (vestibular, haptic, visceral) cues are merged to estimate the orientation of the visual vertical. However, the relative weight of each cue is not fixed, but depends on the specific task. Next, we show that an internal model of the effects of gravity is combined with multisensory signals to time the interception of falling objects, to time the passage through spatial landmarks during virtual navigation, to assess the duration of a gravitational motion, and to judge the naturalness of periodic motion under gravity

Filling gaps in visual motion for target capture

A remarkable challenge our brain must face constantly when interacting with the environment is represented by ambiguous and, at times, even missing sensory information. This is particularly compelling for visual information, being the main sensory system we rely upon to gather cues about the external world. It is not uncommon, for example, that objects catching our attention may disappear temporarily from view, occluded by visual obstacles in the foreground. Nevertheless, we are often able to keep our gaze on them throughout the occlusion or even catch them on the fly in the face of the transient lack of visual motion information. This implies that the brain can fill the gaps of missing sensory information by extrapolating the object motion through the occlusion. In recent years, much experimental evidence has been accumulated that both perceptual and motor processes exploit visual motion extrapolation mechanisms. Moreover, neurophysiological and neuroimaging studies have identified brain regions potentially involved in the predictive representation of the occluded target motion. Within this framework, ocular pursuit and manual interceptive behavior have proven to be useful experimental models for investigating visual extrapolation mechanisms. Studies in these fields have pointed out that visual motion extrapolation processes depend on manifold information related to short-term memory representations of the target motion before the occlusion, as well as to longer term representations derived from previous experience with the environment. We will review recent oculomotor and manual interception literature to provide up-to-date views on the neurophysiological underpinnings of visual motion extrapolation

Corrigendum: Foot Placement Characteristics and Plantar Pressure Distribution Patterns during Stepping on Ground in Neonates

[This corrects the article on p. 784 in vol. 8, PMID: 29066982.]

Foot Placement Characteristics and Plantar Pressure Distribution Patterns during Stepping on Ground in Neonates

Stepping on ground can be evoked in human neonates, though it is rather irregular and stereotyped heel-to-toe roll-over pattern is lacking. Such investigations can provide insights into the role of contact- or load-related proprioceptive feedback during early development of locomotion. However, the detailed characteristics of foot placements and their association with motor patterns are still incompletely documented. We elicited stepping in 33 neonates supported on a table. Unilateral limb kinematics, bilateral plantar pressure distribution and EMG activity from up to 11 ipsilateral leg muscles were recorded. Foot placement characteristics in neonates showed a wide variation. In ~25% of steps, the swinging foot stepped onto the contralateral foot due to generally small step width. In the remaining steps with separate foot placements, the stance phase could start with forefoot (28%), midfoot (47%), or heel (25%) touchdowns. Despite forefoot or heel initial contacts, the kinematic and loading patterns markedly differed relatively to toe-walking or adult-like two-peaked vertical force profile. Furthermore, while the general stepping parameters (cycle duration, step length, range of motion of proximal joints) were similar, the initial foot contact was consistently associated with specific center-of-pressure excursion, range of motion in the ankle joint, and the center-of-activity of extensor muscles (being shifted by ~5% of cycle toward the end of stance in the "heel" relative to "forefoot" condition). In sum, we found a variety of footfall patterns in conjunction with associated changes in motor patterns. These findings suggest the potential contribution of load-related proprioceptive feedback and/or the expression of variations in the locomotor program already during early manifestations of stepping on ground in human babies