Interaction of visual and proprioceptive feedback during adaptation of human reaching movements

People tend to make straight and smooth hand movements when reaching for an object. These trajectory features are resistant to perturbation, and both proprioceptive as well as visual feedback may guide the adaptive updating of motor commands enforcing this regularity. How is information from the two senses combined to generate a coherent internal representation of how the arm moves? Here we show that eliminating visual feedback of hand-path deviations from the straight-line reach (constraining visual feedback of motion within a virtual, "visual channel") prevents compensation of initial direction errors induced by perturbations. Because adaptive reduction in direction errors occurred with proprioception alone, proprioceptive and visual information are not combined in this reaching task using a fixed, linear weighting scheme as reported for static tasks not requiring arm motion. A computer model can explain these findings, assuming that proprioceptive estimates of initial limb posture are used to select motor commands for a desired reach and visual feedback of hand-path errors brings proprioceptive estimates into registration with a visuocentric representation of limb position relative to its target. Simulations demonstrate that initial configuration estimation errors lead to movement direction errors as observed experimentally. Registration improves movement accuracy when veridical visual feedback is provided but is not invoked when hand-path errors are eliminated. However, the visual channel did not exclude adjustment of terminal movement features maximizing hand-path smoothness. Thus visual and proprioceptive feedback may be combined in fundamentally different ways during trajectory control and final position regulation of reaching movements.     

Locomotor adaptation to resistance during treadmill training transfers to overground walking in human SCI

Treadmill training has been used as a promising technique to improve overground walking in patients with spinal cord injury (SCI). Previous findings showed that a gait pattern may adapt to a force perturbation during treadmill training and show aftereffects following removal of the force perturbation. We hypothesized that aftereffects would transfer to overground walking to a greater extent when the force perturbation was resisting rather than assisting leg swing during treadmill training. Ten subjects with incomplete SCI were recruited into this study for two treadmill training sessions: one using swing resistance and the other using swing assistance during treadmill stepping. A controlled resistance/assistance was provided to the subjects’ right knee using a customized cable-driven robot. The subjects’ spatial and temporal parameters were recorded during the training. The same parameters during overground walking were also recorded before and after the training session using an instrumented walkway. Results indicated that stride length during treadmill stepping increased following the release of resistance load and the aftereffect transferred to overground walking. In contrast, stride length during treadmill stepping decreased following the release of assistance load, but the aftereffect did not transfer to overground walking. Providing swing resistance during treadmill training could enhance the active involvement of the subjects in the gait motor task, thereby aiding in the transfer to overground walking. Such a paradigm may be useful as an adjunct approach to improve the locomotor function in patients with incomplete SCI.     

Unique characteristics of motor adaptation during walking in young children

Children show precocious ability in the learning of languages; is this the case with motor learning? We used split-belt walking to probe motor adaptation (a form of motor learning) in children. Data from 27 children (ages 8-36 mo) were compared with those from 10 adults. Children walked with the treadmill belts at the same speed (tied belt), followed by walking with the belts moving at different speeds (split belt) for 8-10 min, followed again by tied-belt walking (postsplit). Initial asymmetries in temporal coordination (i.e., double support time) induced by split-belt walking were slowly reduced, with most children showing an aftereffect (i.e., asymmetry in the opposite direction to the initial) in the early postsplit period, indicative of learning. In contrast, asymmetries in spatial coordination (i.e., center of oscillation) persisted during split-belt walking and no aftereffect was seen. Step length, a measure of both spatial and temporal coordination, showed intermediate effects. The time course of learning in double support and step length was slower in children than in adults. Moreover, there was a significant negative correlation between the size of the initial asymmetry during early split-belt walking (called error) and the aftereffect for step length. Hence, children may have more difficulty learning when the errors are large. The findings further suggest that the mechanisms controlling temporal and spatial adaptation are different and mature at different times.     

Retinal network adaptation to bright light requires tyrosinase

The visual system adjusts its sensitivity to a wide range of light intensities. We report here that mutation of the zebrafish sdy gene, which encodes tyrosinase, slows down the onset of adaptation to bright light. When fish larvae were challenged with periods of darkness during the day, the sdy mutants required nearly an hour to recover optokinetic behavior after return to bright light, whereas wild types recovered within minutes. This behavioral deficit was phenocopied in fully pigmented fish by inhibiting tyrosinase and thus does not depend on the absence of melanin pigment in sdy. Electroretinograms showed that the dark-adapted retinal network recovers sensitivity to a pulse of light more slowly in sdy mutants than in wild types. This failure is localized in the retinal neural network, postsynaptic to photoreceptors. We propose that retinal pigment epithelium (which normally expresses tyrosinase) secretes a modulatory factor, possibly L-DOPA, which regulates light adaptation in the retinal circuitry.     

Purkinje cells in the lateral cerebellum of the cat encode visual events and target motion during visually guided reaching

In this study the receipt of visual information by the lateral cerebellum and its contribution to a motor output was studied using single unit recording of cerebellar cortical neurones in cats trained to perform visually guided reaching. The activity of Purkinje cells and other cortical neurones in the lateral cerebellum was investigated in relation to various aspects of the task, such as visual events, parameters of target movement, and limb and eye movements. Two-thirds (66%) of Purkinje cells tested could signal simple visual events, such as a flash of light. Neurones were also capable of detecting other less potent, but behaviourally important visual events, such as a 'GO' signal (LED brightening). Half of the cells tested were responsive to the on-going motion of the visual target, displaying tonically altered discharge rates for as long as it was moving, and a 'preferred' target velocity. A small proportion of cells showed short latency visual modulation that persisted during the forelimb reach. Anatomical tracing studies confirmed that the recordings were obtained from the D1 zone of crus I. In summary, cells in this region of lateral cerebellar cortex perform simple visual functions, such as event detection, but also more complex visual functions, such as encoding parameters of target motion, and their visual responsiveness is appropriate for a role in accurate visually guided reaching to a moving target.     

Prism adaptation with delayed visual error signals in the monkey

Errors in reaching produced by displacing the visual field with wedge prisms decrease with trials, even when the error is not revealed until the completion of the movement. To examine how much additional delay in visual feed-back the monkey can compensate for, the effects of delaying the visual error signals were studied by presenting the terminal visual images after one of five delays, ranging from 0 to 500 ms. Adaptation was fastest when the delay was 0 or 10 ms, decreased significantly with a delay as small as 50 ms and approached zero when the delay was 500 ms. The size of the after-effect decreased with the delay accordingly. The results indicate that prism adaptation in the monkey critically depends on the availability of visual information within 50 ms of completion of the movement. Comparing the results with those for humans, we suggest that monkey and human share a mechanism of adaptation with a short time window of 50 ms, but the monkey lacks another mechanism of adaptation that allows a visual delay of 500 ms or more in humans.     

Long-term adaptation to dynamics of reaching movements: a PET study

Positron emission tomography (PET) was used to examine changes in the cerebellum as subjects learned to make movements with their right arm while holding the handle of a robot that produced a force field. Brain images were acquired during learning and then during recall at 2 and 4 weeks. We also acquired images during a control task where the force field was not learnable and subjects did not show any improvements across sessions. During the 1st day, we observed that motor errors decreased from the control condition to the learning condition. However, regional cerebral blood flow (rCBF) in the posterior region of the right cerebellar cortex initially increased from the control condition and then gradually declined with reductions in motor error. Correspondingly, rCBF in the ipsilateral deep cerebellar nuclei (DCN) initially decreased from the control condition and then increased with reductions in motor error. If measures of rCBF mainly reflect presynaptic activity of neurons, this result predicts that DCN neurons fire with a pattern that starts high in the control task then decreases as learning proceeds. Similarly, Purkinje cells should generally have their lowest activity in the control task. This pattern is consistent with neurophysiological recordings that find that cerebellar activity during early learning of a motor task may mainly reflect changes in coactivation of muscles of the limbs, rather than a learning specific signal. By the end of the first session, motor errors had reached a minimum and no further improvements were observed. However, across the weeks a region in the anterior cerebellar cortex showed gradual decreases in rCBF that could not be attributed to changes in motor performance. Because patterns of rCBF in the cortex and nuclei were highly anti-correlated, we used structural equation modeling to estimate how synaptic activity in the cerebellar cortex influenced synaptic activity in the DCN. We found a negative correlation with a strength that significantly increased during the 4 weeks. This suggests that, during long-term recall, the same input to the cerebellar cortex would produce less synaptic activity at the DCN, possibly because of reduced cerebellar cortex output to the DCN.     

Rapid changes in corticospinal excitability during force field adaptation of human walking

Force field adaptation of locomotor muscle activity is one way of studying the ability of the motor control networks in the brain and spinal cord to adapt in a flexible way to changes in the environment. Here, we investigate whether the corticospinal tract is involved in this adaptation. We measured changes in motor-evoked potentials (MEPs) elicited by transcranial magnetic stimulation (TMS) in the tibialis anterior (TA) muscle before, during, and after subjects adapted to a force field applied to the ankle joint during treadmill walking. When the force field assisted dorsiflexion during the swing phase of the step cycle, subjects adapted by decreasing TA EMG activity. In contrast, when the force field resisted dorsiflexion, they increased TA EMG activity. After the force field was removed, normal EMG activity gradually returned over the next 5 min of walking. TA MEPs elicited in the early swing phase of the step cycle were smaller during adaptation to the assistive force field and larger during adaptation to the resistive force field. When elicited 5 min after the force field was removed, MEPs returned to their original values. The changes in TA MEPs were larger than what could be explained by changes in background TA EMG activity. These effects seemed specific to walking, as similar changes in TA MEP were not seen when seated subjects were tested during static dorsiflexion. These observations suggest that the corticospinal tract contributes to the adaptation of walking to an external force field.     

Task goals influence online corrections and adaptation of reaching movements

Everyday movements often have multiple solutions. Many of these solutions arise from biomechanical redundancies. Often, however, the goal does not require a unique movement. To examine how people exploit task-related redundancy, we observed as participants produced three-dimensional (3-D) reaching movements, moving to one of two rectangular targets that were diagonally oriented in the frontal (x, y) plane. On most trials, the movement was perturbed by a vertical, velocity-dependent force. Since participants were free to move in 3-D space, online corrections could involve movement along the perturbed, vertical dimension, as well as the nonperturbed, horizontal dimension. If the motor system exploits task redundancies, then corrections along the horizontal dimension should depend on the orientation of the target. Consistent with this prediction, participants modified both the horizontal and vertical coordinates of the trajectory over the course of learning, and the horizontal component was sensitive to the orientation of the target. Furthermore, participants produced online corrections with a horizontal component that brought the hand closer to the target. These results suggest that we not only correct for mismatches between expected and experienced forces but also exploit task-specific redundancies to efficiently improve performance.     

Prism adaptation of underhand throwing: Rotational inertia and the primary and latent aftereffects

The effect of prism adaptation on movement is typically reduced when movement at test (with prisms removed) is different from movement at training. Previous research [J. Fernández-Ruiz, C. Hall-Haro, R. Díaz, J. Mischner, P. Vergara, J. C. Lopez-Garcia, Learning motor synergies makes use of information on muscular load, Learning & Memory 7 (2000) 193–198] suggests, however, that some adaptation is latent and only revealed through further testing in which the movement at training is fully reinstated. Movement in their training trials was throwing overhand to a vertical target with a mass attached to the arm. The critical test trials involved the same act initially without the attached mass and then with the attached mass. In replication, we studied throwing underhand to a horizontal target with left shifting prisms and a dissociation of the throwing arm's mass and moment of inertia. The two main results were that the observed latent aftereffect (a) depended on the similarity of training and test moments of inertia, and (b) combined with the primary aftereffect to yield a condition-independent sum. Discussion focused on a parallel between prism adaptation and principles governing recall highlighted in investigations of implicit memory: whether given training (study) conditions lead to good or poor persistence of adaptation (memory performance) at test depends on the conditions at test relative to the conditions at training (study).     

Postural responses to unexpected perturbations of balance during reaching

To study the interaction between feedforward and feedback modes of postural control, we investigated postural responses during unexpected perturbations of the support surface that occurred during forward reaching in a standing position. We examined postural responses in lower limb muscles of nine human subjects. Baseline measures were obtained when subjects executed reaching movements to a target placed in front of them (R condition) and during postural responses to forward and backward support-surface perturbations (no reaching, P condition) during quiet stance. Perturbations were also given at different delays after the onset of reaching movements (RP conditions) as well as with the arm extended in the direction of the target, but not reaching (P/AE condition). Results showed that during perturbations to reaching (RP), the initial automatic postural response, occurring around 100 ms after the onset of perturbations, was relatively unchanged in latency or amplitude compared to control conditions (P and P/AE). However, longer latency postural responses were modulated to aid in the reaching movements during forward perturbations but not during backward perturbations. Our results suggest that the nervous system prioritizes the maintenance of a stable postural base during reaching, and that later components of the postural responses can be modulated to ensure the performance of the voluntary task.     

C-Deoxyglucose mapping of the monkey brain during reaching to visual targets

The strategies used by the macaca monkey brain in controlling the performance of a reaching movement to a visual target have been studied by the quantitative autoradiographic ¹⁴C-DG method.Experiments on visually intact monkeys reaching to a visual target indicate that V1 and V2 convey visuomotor information to the cortex of the superior temporal and parietoccipital sulci which may encode the position of the moving forelimb, and to the cortex in the ventral part and lateral bank of the intraparietal sulcus which may encode the location of the visual target. The involvement of the medial bank of the intraparietal sulcus in proprioceptive guidance of movement is also suggested on the basis of the parallel metabolic effects estimated in this region and in the forelimb representations of the primary somatosensory and motor cortices. The network including the inferior postarcuate skeletomotor and prearcuate oculomotor cortical fields and the caudal periprincipal area 46 may participate in sensory-to-motor and oculomotor-to-skeletomotor transformations, in parallel with the medial and lateral intraparietal cortices.Experiments on split brain monkeys reaching to visual targets revealed that reaching is always controlled by the hemisphere contralateral to the moving forelimb whether it is visually intact or ‘blind'. Two supplementary mechanisms compensate for the ‘blindness' of the hemisphere controlling the moving forelimb. First, the information about the location of the target is derived from head and eye movements and is sent to the ‘blind' hemisphere via inferior parietal cortical areas, while the information about the forelimb position is derived from proprioceptive mechanisms and is sent via the somatosensory and superior parietal cortices. Second, the cerebellar hemispheric extensions of vermian lobules V, VI and VIII, ipsilateral to the moving forelimb, combine visual and oculomotor information about the target position, relayed by the ‘seeing' cerebral hemisphere, with sensorimotor information concerning cortical intended and peripheral actual movements of the forelimb, and then send this integrated information back to the motor cortex of the ‘blind' hemisphere, thus enabling it to guide the contralateral forelimb to the target.     

Control of foot trajectory in walking toddlers: adaptation to load changes

On earth, body weight is an inherent constraint, and accordingly, load-regulating mechanisms play an important role in terrestrial locomotion. How do toddlers deal with the effects of their full body weight when faced with the task of independent upright locomotion for the first time? Here we studied the effect of load variation on walking in 12 toddlers during their first unsupported steps, 15 older children (1.3-5 yr), and 10 adults. To simulate various levels of body weight, an experimenter held the trunk of the subject with both hands and supplied an approximately constant vertical force during stepping on a force platform. During unsupported stepping, the shape of the foot path in toddlers (typically single-peak toe trajectory) was different from that of adults and older children (double-peak trajectory). In contrast to adults and older children, who showed only limited changes in kinematic coordination, the "reduced-gravity" condition considerably affected the shape of the foot path in toddlers: they tended to make a high lift and forward foot overshoot at the end of swing. In addition, stepping at high levels of body unloading was characterized by a significant change in the initial direction of foot motion during early swing. Intermediate walkers (1.5-5 mo after walking onset) showed only partial improvement in foot trajectory characteristics. The results suggest that, at the onset of walking, changes in vertical body loads are not compensated accurately by the kinematic controllers; compensation necessitates a few months of independent walking experience.     

Mechanical and physiological effects of varying pole weights during Nordic walking compared to walking

The study investigated the effect of varying pole weights on energy expenditure, upper limb muscle activation and on forces transmitted to the poles during Nordic walking (NW). Twelve women [age = 21 (2) years, body mass = 60.8 (6) kg, height = 1.71 (0.06) m] participated in five 7-min walking tests randomly chosen without poles (W), with normal NW poles (NW) or with added masses of 0.5 kg (NW + 0.5) 1.0 kg (NW + 1.0) or 1.5 kg (NW + 1.5) at a speed of 2 m s⁻¹. Heart rate (HR), relative oxygen uptake ( r[(V)\dot]\textO₂ \hbox{r}\dot{V}{\text{O}}_{2} ), blood lactate (La) and rate of perceived exertion (RPE) were registered along with surface EMG (SEMG) from biceps brachii, triceps brachii, trapecius and deltoideus muscles. Inbuilt force transducers measured reaction forces along the long axes of the poles. NW + 0.5 and NW + 1.5 showed significant increases for r[(V)\dot]\textO₂ \hbox{r}\dot{V}{\text{O}}_{2} and RPE compared with W (p < 0.05) but with no respective differences within NW. SEMG revealed higher activation of biceps brachii for all NW tests plus added masses compared to W (p < 0.05). Additionally the activation of biceps brachii was higher for NW + 1.5 compared to NW (p < 0.05). The contribution to overall activation duration of triceps brachii became lower but increased for biceps brachii with heavier poles. The increased energy expenditure during NW can be attributed to intensified muscle activation during forward swing of the poles. Heavier poles have no effect on energy expenditure compared to NW with usual poles but enhance muscular activity. Since there are no benefits concerning physiological and biomechanical parameters we do not recommend the use of heavier NW poles.     

On the potential role of the corticospinal tract in the control and progressive adaptation of the soleus h-reflex during backward walking

When untrained subjects walk backward on a treadmill, an unexpectedly large amplitude soleus H-reflex occurs in the midswing phase of backward walking. We hypothesized that activity in the corticospinal tract (CST) during midswing depolarizes the soleus alpha-motoneurons subliminally and thus brings them closer to threshold. To test this hypothesis, transcranial magnetic stimulation (TMS) was applied to the leg area of the motor cortex (MCx) during backward walking. Motor-evoked potentials (MEPs) were recorded from the soleus and tibialis anterior (TA) muscles in untrained subjects at different phases of the backward walking cycle. We reasoned that if soleus MEPs could be elicited in midswing, while the soleus is inactive, this would be strong evidence for increased postsynaptic excitability of the alpha-motoneurons. In the event, we found that in untrained subjects, despite the presence of an unexpectedly large H-reflex in midswing, no soleus MEPs were observed at that time. The soleus MEPs were in phase with the soleus electromyographic (EMG) activity during backward walking. Soleus MEPs increased more rapidly as a function of the EMG activity during voluntary activity than during backward walking. Furthermore, a conditioning stimulus to the motor cortex facilitated the soleus H-reflex at rest and during voluntary plantarflexion but not in the midswing phase of backward walking. With daily training at walking backward, the time at which the H-reflex began to increase was progressively delayed until it coincided with the onset of soleus EMG activity, and its amplitude was considerably reduced compared with its value on the first experimental day. By contrast, no changes were observed in the timing or amplitude of soleus MEPs with training. Taken together, these observations make it unlikely that the motor cortex via the CST is involved in control of the H-reflex during the backward step cycle of untrained subjects nor in its progressive adaptation with training. Our observations raise the possibility that the large amplitude of H-reflex in untrained subjects and its adaptation with training are mainly due to control of presynaptic inhibition of Ia-afferents by other descending tracts.     

Split-belt walking: adaptation differences between young and older adults

Human walking is highly adaptable, which allows us to walk under different circumstances. With aging, the probability of falling increases, which may partially be due to a decreased ability of older adults to adapt the gait pattern to the needs of the environment. The literature on visuomotor adaptations during reaching suggests, however, that older adults have little problems in adapting their motor behavior. Nevertheless, it may be that adaptation during a more complex task like gait is compromised by aging. In this study, we investigated the ability of young (n = 8) and older (n = 12) adults to adapt their gait pattern to novel constraints with a split-belt paradigm. Findings revealed that older adults adapted less and more slowly to split-belt walking and showed fewer aftereffects than young adults. While young adults showed a fast adjustment of the relative time spent in swing for each leg older adults failed to do so, but instead they were very fast in manipulating swing speed differences between the two legs. We suggest that these changes in adaptability of gait due to aging stem from a mild degradation of cortico-cerebellar pathways (reduced adaptability) and cerebral structures (decreased ability to change gait cycle timing). However, an alternative interpretation may be that the observed reduced adaptation is a compensatory strategy in view of the instability induced by the split-belt paradigm.     

Kinematic and non-kinematic signals transmitted to the cat cerebellum during passive treadmill stepping

Previous work from this laboratory has shown that activity in the dorsal spinocerebellar tract (DSCT) relates strongly to global hindlimb kinematics variables during passive displacements of the hindlimb. A linear relationship to limb axis orientation and length variables accounts for most of the response variance for passive limb positioning and movement. Here we extend those observations to more natural movements by examining the information carried by the DSCT during passive stepping movements on a treadmill, and we compare it to information transmitted during passive robot-driven hindlimb movements. Using a principal component analysis approach, we found that a linear relationship between the responses and hindlimb kinematics was comparable across experimental conditions. We also observed systematic non-linearities in this relationship for both types of movement that could be attributed to events corresponding to the touch-down and lift-off phases of the movement. We concluded that proprioceptive information transmitted to the cerebellum by the DSCT during locomotion has at least two major components. One component is associated with limb kinematics (limb orientation) and may be more or less related to the metrics of the step (stride length, for example) or its velocity. The other component is associated with limb length and/or limb loading, and it may signal some aspect of limb stiffness.