Contribution of vision to postural behaviors during continuous support-surface translations

During standing balance, kinematics of postural behaviors have been previously observed to change across visual conditions, perturbation amplitudes, or perturbation frequencies. However, experimental limitations only allowed for independent investigation of such parameters. Here, we adapted a pseudorandom ternary sequence (PRTS) perturbation previously used in rotational support-surface perturbations (Peterka in J Neurophysiol 88(3):1097–1118, 2002) to a translational paradigm, allowing us to concurrently examine the effects of vision, perturbation amplitude, and frequency on balance control. Additionally, the unpredictable PRTS perturbation eliminated effects of feedforward adaptations typical of responses to sinusoidal stimuli. The PRTS perturbation contained a wide spectral bandwidth (0.08–3.67 Hz) and was scaled to 4 different peak-to-peak amplitudes (3–24 cm). Root mean square (RMS) of hip displacement and velocity increased relative to RMS ankle displacement and velocity in the absence of vision across all subjects, especially at higher perturbation amplitudes. Gain and phase lag of center of mass (CoM) sway relative to the perturbation also increased with perturbation frequency; phase lag further increased when vision was absent. Together, our results suggest that visual input, perturbation amplitude, and perturbation frequency can concurrently and independently modulate postural strategies during standing balance. Moreover, each factor contributes to the difficulty of maintaining postural stability; increased difficulty evokes a greater reliance on hip motion. Finally, despite high degrees of joint angle variation across subjects, CoM measures were relatively similar across subjects, suggesting that the CoM is an important controlled variable for balance.     

A feedback model reproduces muscle activity during human postural responses to support-surface translations

Although feedback models have been used to simulate body motions in human postural control, it is not known whether muscle activation patterns generated by the nervous system during postural responses can also be explained by a feedback control process. We investigated whether a simple feedback law could explain temporal patterns of muscle activation in response to support-surface translations in human subjects. Previously, we used a single-link inverted-pendulum model with a delayed feedback controller to reproduce temporal patterns of muscle activity during postural responses in cats. We scaled this model to human dimensions and determined whether it could reproduce human muscle activity during forward and backward support-surface perturbations. Through optimization, we found three feedback gains (on pendulum acceleration, velocity, and displacement) and a common time delay that allowed the model to best match measured electromyographic (EMG) signals. For each muscle and each subject, the entire time courses of EMG signals during postural responses were well reconstructed in muscles throughout the lower body and resembled the solution derived from an optimal control model. In ankle muscles, >75% of the EMG variability was accounted for by model reconstructions. Surprisingly, >67% of the EMG variability was also accounted for in knee, hip, and pelvis muscles, even though motion at these joints was minimal. Although not explicitly required by our optimization, pendulum kinematics were well matched to subject center-of-mass (CoM) kinematics. Together, these results suggest that a common set of feedback signals related to task-level control of CoM motion is used in the temporal formation of muscle activity during postural control.     

Development of postural adaptation to arm raising

We studied the development of the coordination between posture and movement by analyzing the shifts of the center of pressure (CoP) associated with arm raising. Three groups of children aged 3–5 years, 6–8 years, and 9–10 years and an adult group were tested. The subjects were required to raise their arms to the horizontal position while standing still, with their hands free or loaded (5% of the body weight). The arm movements were recorded by a TV-image processor, and the changes in position of the CoP were measured by a force platform and analyzed before, during, and after the arm movement. The data show that the CoP moved forward during arm raising, that additional load induced a greater shift in all age groups, and that the relative amplitude of the shift decreased with age. The greatest changes occurred between ages 3–5 years and 6–8 years. The pre- and postmovement CoP shift suggests qualitative changes in the postural adaptation to movement between these two age groups: the anticipatory postural adjustments moved from a supporting function to a compensatory function, yielding an increasing functional convergence between the feedforward and the feedback modes of postural control, and an increasing rapidness in recovering postural stability after arm movement. The postural behavior shown by the 9- to 10-year-old children and by the adults in the arms-free condition suggests an increased tolerance to unbalance when postural oscillations do not jeopardize static equilibrium. Electronic Publication     

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.     

Reaching movements: mode of motor programming influences programming time by itself

The present study was undertaken to assess the effect of both target spatial dispersion and mode of motor programming (an implicit strategy, continuous or discrete) on the time needed to initiate accurate arm reaching trajectories. For this purpose, we compared three conditions, in which human subjects were required to reach to one of four possible targets, equidistant from a common origin, in four different directions. The directions were varied across conditions in such a way that (1) the total spatial dispersion of targets varied, or (2) the separations between the medial targets varied, or (3) both (1) and (2) varied. We confirmed that a wider target spatial dispersion determines a lengthening of programming time. The major finding of this work is that, even when target spatial dispersion is kept constant, the continuous mode of programming allows a faster specification of the correct trajectory, while the discrete mode yields a slower programming process. Thus, the mode of motor programming influences the programming time course by itself. Electronic Publication     

Saccade adaptation in response to altered arm dynamics

The delays in sensorimotor pathways pose a formidable challenge to the implementation of stable error feedback control, and yet the intact brain has little trouble maintaining limb stability. How is this achieved? One idea is that feedback control depends not only on delayed proprioceptive feedback but also on internal models of limb dynamics. In theory, an internal model allows the brain to predict limb position. Earlier we had found that during reaching, the brain estimates hand position in real-time in a coordinate system that can be used for generating saccades. Here we tested the idea that the estimate of hand position, as expressed through saccades, depends on an internal model that adapts to dynamics of the arm. We focused on the behavior of the eyes as perturbations were applied to the unseen hand. We found that when the hand was perturbed from stable posture with a 100-ms force pulse of random direction and magnitude, a saccade was generated on average at 182 ms postpulse onset to a position that was an unbiased estimate of real-time hand position. To test whether planning of saccades depended on an internal model of arm dynamics, arm dynamics were altered either predictably or unpredictably during the postpulse period. When arm dynamics were predictable, saccade amplitudes changed to reflect the change in the arm's behavior. We suggest that proprioceptive feedback from the arm is integrated into an adaptable internal model that computes an estimate of current hand position in eye-centered coordinates.     

Fast voluntary trunk flexion movements in standing: primary movements and associated postural adjustments

Movement patterns were studied during fast voluntary forward flexions of the trunk from an erect standing position. Three healthy subjects performed three series of six consecutive trunk flexions at maximum velocity and with successively increasing amplitude, covering a major part of the range of motion (range for all subjects: 13-97 degrees). Angular displacements of the trunk, hip, knee and ankle were measured together with the tilt of the pelvis and the flexion of the spine using a Selspot optoelectronic system. Trunk flexion was the result of a simultaneous forward pelvic tilt and flexion of the spine. For trunk movements up to 55 degrees, spine flexion dominated the movement, whereas for larger movements a major part of the amplitude was caused by pelvic tilt. During flexion of the trunk a simultaneous hip flexion and ankle extension was seen. At the knee there was an initial flexion and a subsequent extension. The net amplitude of the knee flexion showed a negative correlation with net trunk flexion amplitude for movements up to 50 degrees, whereas for larger amplitudes the correlation was positive. Time from onset of the trunk movement to peak knee flexion showed a weak correlation to net trunk flexion amplitude (r = 0.34) whereas the corresponding correlation was higher for pelvic tilt, spine flexion, hip flexion, ankle extension, and knee extension (r = 0.60-0.91). Each successive trial during a series of trunk movements was started from an increasing degree of knee flexion. This gradual adaptation was also present when successive trunk flexions were performed with constant movement amplitude.(ABSTRACT TRUNCATED AT 250 WORDS)     

Long-term adaptation of postural control in microgravity

Orbital microgravity represents a unique environment, which allows the isolation of variables assumed to be involved in the mechanism of body positioning in space. In this context, the alignment of the trunk axis along allocentric references and the positioning of the body center of mass inside the supporting base compete for the role of the primary-controlled variable when assuming erect posture. This paper reports the quantitative evaluation of the postural strategies exhibited by two subjects with feet fixed to the floor of the space module along a 4-month period of exposure to microgravity. With respect to previous findings in parabolic flights and short term space missions, the analysis focused on long-term process of sensorimotor adaptation to weightlessness. Results show that while trunk-axis orientation is preserved and used as a stable postural frame of reference, the positioning of the body center of mass appears to be significantly biased backward and turns out to be involved in a long-term process of adaptation throughout the entire flight towards the re-emergence of a typically terrestrial postural regulation compatible with equilibrium. Received: 30 July 1998 / Accepted: 30 April 1999     

Contribution of signals downstream from adaptation to saccade programming

Information about ongoing behavior is necessary for stable perception and subsequent motor planning. Although many recurrent networks are known in the motor systems, the pathways that transmit the signals for internal monitoring of behavior are not specified. The present study reports that the pathways originating from sites downstream of cerebellar adaptation provide internal signals that are used for subsequent eye-movement programming. When monkeys made two successive saccades toward the locations of previously flashed targets or initial fixation, the second saccade compensated for the adaptive changes in the primary saccade. The use of signals downstream from adaptation for saccade programming contrasts with recent findings that signals upstream from adaptation control the perceptual localization of visual stimuli presented around the time of saccade, suggesting that separate recurrent networks provide behavioral information for perception versus movement programming.     

Bimanual adaptation: internal representations of bimanual rhythmic movements

From tying your shoes and clipping your tie to the claps at the end of a fine seminar, bimanual coordination plays a major role in our daily activities. An important phenomenon in bimanual coordination is the predisposition toward mirror symmetry in the performance of bimanual rhythmic movements. Although learning and adaptation in bimanual coordination are phenomena that have been observed, they have not been studied in the context of adaptive control and internal representations—approaches that were successfully employed in the arena of reaching movements and adaptation to force perturbations. In this paper we examine the dynamics of the learning mechanisms involved when subjects are trained to perform a bimanual non-harmonic polyrhythm in a bimanual index finger tapping task. Subjects are trained in this task implicitly, using altered visual feedback, while their performance is continuously monitored throughout the experiment. Our experimental results indicate the existence of significant (p<<0.01) learning curves (i.e., error plots with significantly negative slopes) during training and aftereffects with a washout period after the visual feedback ceases to be altered. These results confirm the formation of internal representations in bimanual motor control. We present a simple, physiologically plausible, neural model that combines feedback and adaptation in the control process and which is able to reproduce key phenomena of bimanual coordination and adaptation.     

Directional specificity of postural muscles in feed-forward postural reactions during fast voluntary arm movements

Healthy subjects performed bilateral fast shoulder movements in different directions while standing on a force platform. Anticipatory postural adjustments were seen as changes in the electrical activity of postural muscles as well as displacements of the center of pressure and center of gravity. Postural muscle pairs of agonist-antagonist commonly demonstrated triphasic patterns starting prior to the first electromyographic (EMG) burst in the prime-mover muscle. Proximal postural muscles demonstrated the largest anticipatory increase in the background activity during movements in one of the two opposite directions (forward or backwards). These changes progressively decreased when movements deviated from the preferred direction and frequently disappeared during movements in the opposite direction. The patterns in distal muscles varied across subjects and could demonstrate larger anticipatory changes during movements forward and backwards as compared to movements in intermediate directions. Bilateral addition of inertial loads to the wrists did not change the general anticipatory patterns, while making some of their features more pronounced. Anticipatory postural adjustments were followed by later changes in the activity of postural muscles, also reflected in the mechanical variables. Changes in leg joint angles revealed a hip-ankle strategy during shoulder flexions and an ankle strategy during shoulder extensions. The study demonstrates different behaviors of proximal and distal muscles during anticipatory postural adjustments in preparation for fast arm movements. We suggest that the proximal muscles produce a general pattern of postural adjustments, while distal muscles take care of fine adjustments that are more likely to vary across subjects.     

Central patterning of speech movements

Summary Previous speech kinematic studies have demonstrated systematic timing relations among the upper lip, lower lip, and jaw suggesting the operation of a central pattern generator (CPG). The present study evaluated the consistency of these timing relations following unanticipated perturbation of the lower lip. Using this approach, it was also possible to evaluate the influence of sensory information on the timing of motor output and subsequent coordination of the multiple speech movements. Perturbations were applied to the lower lip during the closing movement associated with the first p in sapapple. Muscle activity and movements of the upper lip, lower lip, and jaw were obtained. Changes in movement displacement, velocity and duration, the timing and sequencing of peak velocities, EMG area, and EMG rise time were analyzed for the control and load conditions. Similar to previous perturbation results, significant magnitude compensations from the muscles and movements of the upper lip, lower lip, and jaw were observed. In contrast, movement durations and the sequencing of peak velocities were relatively unaffected by the lower lip load. The timing of peak EMG amplitude and consequently the timing of peak closing velocity for all structures (UL, LL, and J) occurred earlier relative to the preceding opening movement. These results are consistent with the interaction of phasic sensory input with centrally-driven commands resulting in a phase-advanced motor output. Further, as the timing of one structure is modified so were all the functionally-linked components thereby maintaining the necessary coordination. As in other rhythmic motor behaviors such as locomotion and chewing, there appears to be a centrally patterned framework for speech movement coordination.     

Postural synergies in axial movements: short and long-term adaptation

Summary Fast backward trunk movements are accompanied by hip, knee and ankle rotation which compensate for the backward shift of the center of gravity. The electromyographic pattern associated with the performance of these movements and the associated synergies consists of a fairly synchronous activation of the prime mover (erectores spinae) and the muscles situated at the back of the leg (hamstring, calf muscles). This pattern is called the non anticipated pattern. The effect of training on the EMG pattern and on the subjects' mechanical performances was investigated by comparing a population of untrained subjects with one of highly trained gymnasts. A new EMG pattern was observed in the highly trained gymnasts, the distally anticipated pattern consisting of an early activation of the gastrocnemius, and in some subjects also of the hamstring, indicating that a long term adaptation had taken place. Performances expressed as a ratio between the displacement of the center of gravity projection onto the ground and the velocity of the movement were clearly better in the gymnasts. Short term adaptation was found to occur in the gymnasts and not in the untrained group when the movement was performed while standing on a narrow support. A suppression of the distal gastrocnemius burst occurred in the gymnasts from the first trial under the constrained standing condition whereas no change occurred in the untrained group. The flexibility of the EMG patterns associated with axial movements occurring either spontaneously or as a result of long or short term training is discussed.     

Morphogenetic adaptation of the looping embryonic heart to altered mechanical loads.

The biophysical mechanisms that drive and regulate cardiac looping are not well understood, but mechanical forces likely play a central role. Previous studies have shown that cardiac torsion, which defines left-right directionality, is caused largely by forces exerted on the heart tube by a membrane called the splanchnopleure (SPL). Here we show that, when the SPL is removed from the embryonic chick heart, torsion is initially suppressed. Several hours later, however, normal torsion is restored. This delayed torsion coincides with increased myocardial stiffness, especially on the right side of the heart. Exposure to the myosin inhibitor Y-27632 suppressed both responses, suggesting that the delayed torsion is caused by an abnormal cytoskeletal contraction. This hypothesis is supported further by computational modeling. These results suggest that the looping embryonic heart has the ability to adapt to changes in the mechanical environment, which may play a regulatory role during morphogenesis.     

The role of eye movements in visuo-manual adaptation

The present study evaluated the role of eye movements for manual adaptation to reversed vision. Subjects tracked a visual target using a mouse-driven cursor. In Experiment A, they were instructed to look at the target, look at the cursor, fixate straight ahead, or received no instructions regarding eye movements (Groups T, C, F, and N, respectively). Experiment B involved Groups T and C only. In accordance with literature, baseline manual tracking was more accurate when subjects were instructed to move their eyes rather than to fixate straight ahead. In contrast, no such benefit was observed for the adaptive improvement of tracking. We therefore concluded that transfer of information from the oculomotor to the hand motor system enhances the ongoing control of hand movements but not their adaptive modification; probably because the large computational demand of adaptation does not allow an additional processing of supplementary oculomotor signals. We further found adaptation to be worse in T than in any other group. In particular, adaptation was worse in T than in C although eye movements were the same: subjects in both groups moved their eyes in close relationship with the target rather than the cursor, Group C thus disobeying our instructions. The deficient performance of Group T is therefore not related to eye movements per se, but rather to our instructions. We conclude that an independently moving target strongly attracts eye movements independent of instruction (i.e. Groups T and C), but instructions may redirect spatially selective attention (i.e. Group T vs C), and thus influence adaptation.     

Rapid adaptation of torso pointing movements to perturbations of the base of support

We investigated whether pointing movements made with the torso would adapt to movement-contingent augmentation or attenuation of their spatial amplitude. The pointing task required subjects standing on a platform in the dark to orient the mid-sagittal plane of their torso to the remembered locations of just extinguished platform-fixed visual targets without moving their feet. Subjects alternated pointing at two chest-high targets, 60° apart, (1) in a baseline period with the stance platform stationary, (2) during exposure to concomitant contra or ipsiversive platform rotations that grew incrementally to 50% of the velocity of torso rotation, and (3) after return in one step to stationary platform conditions. The velocity and amplitude of torso movements relative to space decreased 25–50% during exposure to contraversive platform rotations and increased 20–50% during ipsiversive rotations. Torso rotation kinematics relative to the platform (as well as the platform-fixed targets and feet) remained virtually constant throughout the incremental exposure period. Subjects were unaware of the altered motion of their body in space imposed by the platform and did not perceive their motor adjustments. Upon return to stationary conditions, torso rotation movements were smaller and slower following adaptation to contraversive rotations and larger and faster after ipsiversive platform rotations. These results indicate a rapid sensory-motor recalibration to the altered relationship between spatial (inertial) torso motion and intended torso motion relative to the feet, and rapid re-adaptation to normal conditions. The adaptive system producing such robust torso regulation provides a critical basis for control of arm, head, and eye movements.     

Phase-dependent organization of postural adjustments associated with arm movements while walking

This study examines the interactions between anteroposterior postural responses and the control of walking in human subjects. In the experimental paradigm, subjects walked upon a treadmill, gripping a rigid handle with one hand. Postural responses at different phases of stepping were elicited by rapid arm pulls or pushes against the handle. During arm movements, EMG's recorded the activity of representative arm, ankle, and thigh segment muscles. Strain gauges in the handle measured the force of the arm movement. A Selspot II system measured kinematics of the stepping movements. The duration of support and swing phases were marked by heel and toe switches in the soles of the subjects' shoes. In the first experiment, subjects were instructed to pull on the handle at their own pace. In these trials all subjects preferred to initiate pulls near heel strikes. Next, when instructed to pull as rapidly as possible in response to tone stimuli, reaction times were similar for all phases of the step cycle. Leg muscle responses associated with arm pulls and pushes, referred to as "postural activations," were directionally specific and preceded arm muscle activity. The temporal order and spatial distribution of postural activations in the muscles of the support leg were similar when arm pull movements occurred while the subject was standing in place and after heel strike while walking. Activations began in the ankle and radiated proximally to the thigh and then the arm. Activations of swing leg muscles were also directionally specific and involved flexion and forward or backward thrust of the limb. When arm movements were initiated during transitions from support by one leg to the other, patterns of postural activations were altered. Alterations usually occurred 10-20 ms before hell strikes and involved changes in the timing and sometimes the spatial structure of postural activations. Postural activation patterns are similar during in-place standing and during the support phase of locomotion. Walking and posture control appear to be separately organized but interrelated activities. Our results also suggest that the stepping generators, not peripheral feedback time locked to heel strikes, modulate postural activation patterns.