Functional Synergies Underlying Control of Upright Posture during Changes in Head Orientation

Background

Studies of human upright posture typically have stressed the need to control ankle and hip joints to achieve postural stability. Recent studies, however, suggest that postural stability involves multi degree-of-freedom (DOF) coordination, especially when performing supra-postural tasks. This study investigated kinematic synergies related to control of the body’s position in space (two, four and six DOF models) and changes in the head’s orientation (six DOF model).

Methodology/Principal Findings

Subjects either tracked a vertically moving target with a head-mounted laser pointer or fixated a stationary point during 4-min trials. Uncontrolled manifold (UCM) analysis was performed across tracking cycles at each point in time to determine the structure of joint configuration variance related to postural stability or tracking consistency. The effect of simulated removal of covariance among joints on that structure was investigated to further determine the role of multijoint coordination. Results indicated that cervical joint motion was poorly coordinated with other joints to stabilize the position of the body center of mass (CM). However, cervical joints were coordinated in a flexible manner with more caudal joints to achieve consistent changes in head orientation.

Conclusions/Significance

An understanding of multijoint coordination requires reference to the stability/control of important performance variables. The nature of that coordination differs depending on the reference variable. Stability of upright posture primarily involved multijoint coordination of lower extremity and lower trunk joints. Consistent changes in the orientation of the head, however, required flexible coordination of those joints with motion of the cervical spine. A two-segment model of postural control was unable to account for the observed stability of the CM position during the tracking task, further supporting the need to consider multijoint coordination to understand postural stability.     

No evidence of expertise-related changes in muscle synergies during rowing

The purpose of the present study was to determine whether expertise in rowing is driven by a specific structure in muscular coordination. We compared seven experienced rowers and eight untrained (i.e., inexperienced) subjects during rowing on an ergometer. Both surface electromyography activity and mechanical patterns (forces exerted at the handle and the foot-stretcher) were recorded during a high intensity rowing exercise. A non-negative matrix factorization was applied to 23 electromyographic patterns to differentiate muscle synergies. Results showed that expertise was not associated with different dimensionality in the electromyographic data and that three muscle synergies were sufficient to explain the majority of the variance accounted for (i.e., >90% of the total variance) in the two populations. The synergies extracted were similar in the two populations, with identical functional roles. While the temporal organization of the propulsive synergies was very similar, slight differences were found in the composition of the muscle synergies (muscle synergy vectors) between the two populations. The results suggests that rowing expertise would not require the development of novel muscle synergies but would imply intrinsic synergies already used in different behaviors. Performance in rowing is more probably linked to adjustments in the mechanical output of the muscle synergies rather than to differences in the shape and timing of their activations.     

Neural basis of learning new movements: evolution of classical concepts

According to classical consepts, the role of the motor cortex in performance of skilled movements of distal parts of extremities is confined to control of appropriate motoneurons by the "point-to-point" principle. However, much evidence of plasticity of the motor cortex and its active role in motor learning appeared in last decade. Fos-gene expression in the motor cortex was found to accompany learning a skill. Strengthening of horizontal pathways in layers II-III was revealed, and cholinergic input to tese layers was found to be important. The imaging data show that activity of the motor cortex increases during motor practice as well. This raises the question of specificity of the motor cortex in the motor learning per se. During acquisition of new movements some previously used synergies prevent the necessary coordination from being learned, so they must be suppressed in the process of motor learning. Investigations of central mechanisms of coordination interference in humans are still at the beginning. However, there are some animal models of reorganization and suppression of interfering synergies. The reorganization and suppression of coordination preventing realization of a new movement is shown to be a specific function of the motor cortex. After automation of new synergies the cortical control is still present, as distinct from the learned movements, which do not require suppression of interfering synergies. However, it does not mean that the conscious control of the performance is still present.     

Muscle synergies during bench press are reliable across days

Muscle synergies have been investigated during different types of human movement using nonnegative matrix factorization. However, there are not any reports available on the reliability of the method. To evaluate between-day reliability, 21 subjects performed bench press, in two test sessions separated by approximately 7 days. The movement consisted of 3 sets of 8 repetitions at 60% of the three repetition maximum in bench press. Muscle synergies were extracted from electromyography data of 13 muscles, using nonnegative matrix factorization. To evaluate between-day reliability, we performed a cross-correlation analysis and a cross-validation analysis, in which the synergy components extracted in the first test session were recomputed, using the fixed synergy components from the second test session. Two muscle synergies accounted for >90% of the total variance, and reflected the concentric and eccentric phase, respectively. The cross-correlation values were strong to very strong (r-values between 0.58 and 0.89), while the cross-validation values ranged from substantial to almost perfect (ICC3, 1 values between 0.70 and 0.95). The present findings revealed that the same general structure of the muscle synergies was present across days and the extraction of muscle synergies is thus deemed reliable.     

Evidence of muscle synergies during human grasping

Motor synergies have been investigated since the 1980s as a simplifying representation of motor control by the nervous system. This way of representing finger positional data is in particular useful to represent the kinematics of the human hand. Whereas, so far, the focus has been on kinematic synergies, that is common patterns in the motion of the hand and fingers, we hereby also investigate their force aspects, evaluated through surface electromyography (sEMG). We especially show that force-related motor synergies exist, i.e. that muscle activation during grasping, as described by the sEMG signal, can be grouped synergistically; that these synergies are largely comparable to one another across human subjects notwithstanding the disturbances and inaccuracies typical of sEMG; and that they are physiologically feasible representations of muscular activity during grasping. Potential applications of this work include force control of mechanical hands, especially when many degrees of freedom must be simultaneously controlled.     

Positive work as a function of eccentric load in maximal leg extension movements

Negative and positive work performed during leg extension movements of 53 well trained subjects was measured with the help of a special dynamometer. The subjects performed four maximal push off trials against five different loads (25-105 kg): two two-legged extensions from a squatting position (SM) with a knee angle of 70 degrees and two trials with a preliminary counter movement (CM) but with the same extension range as in the SM. Positive work differed only by about 4% between CM and SM in spite of large differences in initial forces at the onset of concentric contraction. Based on simulations, it is suggested that in CM the advantage of stored elastic energy can almost completely be nullified by the disadvantage of a limited shortening distance of the contractile elements. It is hypothesised that elastic energy in CM can only cause considerable extra work during concentric contraction compared to the maximal positive work done in SM if the total range of lengthening and shortening of the muscle(s) involved is larger in CM than in SM.     

A two-dimensional aerodynamic model of freely flying insects

Possible free flights of insects by a single flapping motion were studied. It is well-known that insects utilize vortices generated by flapping, by which they generate larger lift than that evaluated by the ordinary aerodynamic theory. However, the effect of the motion of the center of mass (CM) of the insect on its flight has not been clarified. To clarify the effect, numerical simulation was performed for a simple model considering the coupling between the vertical CM motion and the separation vortices generated by flapping wing. As a result, it is shown that the flapping flight has the following interesting features. First, despite a single flapping motion, the model exhibits two types of flapping flight: a steady flight in which the CM velocity oscillates and a wandering flight in which the CM velocity varies irregularly. These two types of flights are selected by the initial conditions even when all the parameters are the same. Second, at a certain critical parameter value, the steady flight loses its stability and undergoes an abrupt transition to the wandering flight. Interestingly, at this critical value, the steady flight can be regarded as hovering. The possible flights are analyzed in terms of bifurcation, and the bifurcation structure is qualitatively explained based on a simple assumption. These results suggest the significance of the effect of CM motion.     

Modular neuromuscular control of human locomotion by central pattern generator

The central pattern generators (CPG) in the spinal cord are thought to be responsible for producing the rhythmic motor patterns during rhythmic activities. For locomotor tasks, this involves much complexity, due to a redundant system of muscle actuators with a large number of highly nonlinear muscles. This study proposes a reduced neural control strategy for the CPG, based on modular organization of the co-active muscles, i.e., muscle synergies. Four synergies were extracted from the EMG data of the major leg muscles of two subjects, during two gait trials each, using non-negative matrix factorization algorithm. A Matsuoka׳s four-neuron CPG model with mutual inhibition, was utilized to generate the rhythmic activation patterns of the muscle synergies, using the hip flexion angle and foot contact force information from the sensory afferents as inputs. The model parameters were tuned using the experimental data of one gait trial, which resulted in a good fitting accuracy (RMSEs between 0.0491 and 0.1399) between the simulation and experimental synergy activations. The model׳s performance was then assessed by comparing its predictions for the activation patterns of the individual leg muscles during locomotion with the relevant EMG data. Results indicated that the characteristic features of the complex activation patterns of the muscles were well reproduced by the model for different gait trials and subjects. In general, the CPG- and muscle synergy-based model was promising in view of its simple architecture, yet extensive potentials for neuromuscular control, e.g., resolving redundancies, distributed and fast control, and modulation of locomotion by simple control signals.     

Age-related changes in multifinger synergies in accurate moment of force production tasks.

The purpose of this investigation was to document and quantify age-related differences in the coordination of fingers during a task that required production of an accurate time profile of the total moment of force by the four fingers of a hand. We hypothesized that elderly subjects would show a decreased ability to stabilize a time profile of the total moment of force, leading to larger indexes of moment variability compared with young subjects. The subjects followed a trapezoidal template on a computer screen by producing a time profile of the total moment of force while pressing down on force sensors with the four fingers of the right (dominant) hand. To quantify synergies, we used the framework of the uncontrolled manifold hypothesis. The elderly subjects produced larger total force, larger variance of both total force and total moment of force, and larger involvement of fingers that produced moment of force against the required moment direction (antagonist moment). This was particularly prominent during supination efforts. Young subjects showed covariation of commands to fingers across trials that stabilized the moment of total force (moment-stabilizing synergy), while elderly subjects failed to do so. Both subject groups showed similar indexes of covariation of commands to the fingers that stabilized the time profile of the total force. The lack of moment-stabilizing synergies may be causally related to the documented impairment of hand function with age.     

Involvement of microtubules in the tolerance of cardiomyocytes to cold ischemia-reperfusion

Before transplantation, the heart graft is preserved by the use of cold storage in order to limit ischemia-reperfusion stress. However, sustained exposure to low temperature may induce myocardial ultrastructural damage, particularly microtubules (MT) disruption. Previous data suggested that tubulin-binding agents are able to attenuate cold-induced cytoskeleton alterations. Thus, the aim of the present work was to study the influence of docetaxel (DX, a tubulin-binding taxane) on the effects of deep hypothermia (4°C) and of simulated cold ischemia-reperfusion on the MT network and oxidative stress of cardiomyocyte (CM) in monolayer cultures prepared from newborn rat ventricles. The MT network was explored by immunocytochemistry and Western-blotting, the cell stress by tetrazolium dye assay (MTT) and lactate dehydrogenase (LDH) release, and the superoxide production by the dihydroethidium probe (DHE). The MT assembly remained stable after 4 and 8 h of hypothermia. Tubulin acetylation was promoted in CM subjected to 4-h hypothermia. Low temperature reduced the mitochondrial function and increased the basal LDH release. The cold ischemia during 4 and 8 h preserved MT network. Docetaxel promoted MT polymerization and tubulin acetylation in basal and in cold conditions. This drug decreased the release of LDH induced by cold ischemia. Moreover, hypothermia (4 h) significantly raised the anion superoxide production. Docetaxel decreased this oxidative stress in the control CM and in CM submitted to 4 h of hypothermia. These data demonstrated that stabilizing MT with DX exerted a protective effect on CM subjected to hypothermia and to cold ischemia-reperfusion. Tubulin-ligands should be thus considered to improve the tolerance of the heart graft toward stressing conservative conditions.     

The Influence of Dopaminergic Striatal Innervation on Upper Limb Locomotor Synergies

To determine the role of striatal dopaminergic innervation on upper limb synergies during walking, we measured arm kinematics in 13 subjects with Parkinson disease. Patients were recruited according to several inclusion criteria to represent the best possible in vivo model of dopaminergic denervation. Of relevance, we included only subjects with normal spatio-temporal parameters of the stride and gait speed to avoid an impairment of upper limbs locomotor synergies as a consequence of gait impairment per se. Dopaminergic innervation of the striatum was measured by FP-CIT and SPECT. All patients showed a reduction of gait-associated arms movement. No linear correlation was found between arm ROM reduction and contralateral dopaminergic putaminal innervation loss. Still, a partition analysis revealed a 80% chance of reduced arm ROM when putaminal dopamine content loss was >47%. A significant correlation was described between the asymmetry indices of the swinging of the two arms and dopaminergic striatal innervation. When arm ROM was reduced, we found a positive correlation between upper-lower limb phase shift modulation (at different gait velocities) and striatal dopaminergic innervation. These findings are preliminary evidence that dopaminergic striatal tone plays a modulatory role in upper-limb locomotor synergies and upper-lower limb coupling while walking at different velocities.     

Cholinergic stimulation induces asynchrony between the circular and longitudinal muscle contraction during esophageal peristalsis

In healthy subjects, a close temporal correlation exists between contractions of the circular muscle (CM) and longitudinal muscle (LM) layers of the esophagus. Patients with nutcracker esophagus show disassociation between the peak of contractions of the CM and LM layers and the peak of contraction 1-3 s apart (Jung HY, Puckett JL, Bhalla V, Rojas-Feria M, Bhargava V, Liu J, Mittal RK. Gastroenterology 128: 1179-1186, 2005). The purpose of the present study was to evaluate the effect of acetylcholinesterase inhibitor (edrophonium) and acetylcholine receptor antagonist (atropine) on human esophageal peristalsis in normal subjects. High-frequency intraluminal ultrasound imaging and manometry were performed simultaneously during swallow-induced peristalsis in ten normal subjects. Standardized 5-ml water swallows were recorded 2 cm above the lower esophageal sphincter under three study conditions: control, edrophonium (80 microg/kg iv), and atropine (10 microg/kg iv). A close temporal correlation exists between the peak pressure and peak wall thickness during the control period. The mean time lag between the peak LM and peak CM contraction was 0.03 s. After edrophonium administration, the mean contraction amplitude increased from 101 +/- 9 mmHg to 150 +/- 20 mmHg (P < 0.05) and mean peak muscle thickness increased from 3.0 +/- 0.2 mm to 3.6 +/- 0.3 mm (P < 0.01), and duration of both CM and LM contractions were also increased. Furthermore, the mean time difference between the peak LM and CM was increased to 1.1 s, (ranging 0.2 to 3.4 s) (P < 0.0001). We conclude that cholinomimetic agent induces discoordination between the two muscle layers of the esophagus.     

Potential of high‐density pheromone‐releasing microtraps for control of codling moth Cydia pomonella and obliquebanded leafroller Choristoneura rosaceana

Recent large‐cage studies with codling moth Cydia pomonella (L.) reveal that the removal of moths from an apple orchard using pheromone‐releasing traps is more effective at reducing capture in a central monitoring trap than is a mating disruption protocol without kill/capture. The present study uses open orchard 0.2‐ha plots comparing a high‐density trapping scenario with mating disruption to confirm those results. Two tortricid moth pests of tree fruit are studied: codling moth and obliquebanded leafroller Choristoneura rosaceana (Harris). Codling moth treatments include Isomate CM FLEX (ShinEtsu Ltd, Japan), nonsticky traps baited with Trécé CM lures (Trécé, Inc., Adair, Oklahoma), and sticky traps baited with Trécé CM lures, all at equal application rates of 500 dispensers ha^?1, as well as a no pheromone control. These microtraps are of a novel design, small and easy to apply, and potentially inexpensive to produce. Mating disruption using Isomate CM FLEX and nonsticky traps reduces codling moth capture in standard monitoring traps by 58% and 71%, respectively. The attract‐and‐remove treatment with sticky traps reduces capture by 92%. Obliquebanded leafroller treatments include Isomate OBLR/PLR Plus and Pherocon IIB microtraps baited with Trécé OBLR lures, both applied at 500 dispensers ha^?1, as well as a no pheromone control. Mating disruption reduces capture in monitoring traps by 69%. The attract‐and‐remove treatment reduces capture by 85%. Both studies suggest that an attract‐and‐remove approach has the potential to provide superior control of moth populations compared with that achieved by mating disruption operating by competitive attraction.     

Locust flight behavior after hemisection of individual thoracic ganglia: evidence for hemiganglionic premotor centers

Summary The flight behavior of locusts with hemisected mesothoracic or metathoracic ganglia was observed in unrestrained animals and monitored electromyographically in tethered animals. Animals with hemisected mesothoracic ganglia were able to initiate and carry out free flight. Hemisection of the mesothoracic ganglion caused no significant changes in the pattern of flight muscle firing; both intra- and intersegmental coordination of flight muscle activity were retained (Figs. 3, 4). Additional transection of one meso-metathoracic connective altered the pattern of flight muscle firing but did not abolish rhythmic activity (Fig. 8). Deafferentation of the thoracic ganglia in animals with hemisected mesothoracic ganglia resulted in rhythmically coordinated motor activity (Fig. 5) which was indistinguishable from that shown by deafferented animals with all ganglia intact. Hemisection of the metathoracic ganglion resulted in an abnormal pattern of flight muscle firing. However, a basic rhythmicity of motor activity was still present (Fig. 6). The implications of these results for rhythm generation and motor coordination in the flight control system of the locust are discussed.     

Anthropomorphic Control of a Dexterous Artificial Hand via Task Dependent Temporally Synchronized Synergies

Despite the recent influx of increasingly dexterous prostheses, there remains a lack of sufficiently intuitive control methods to fully utilize this dexterity. As a solution to this problem, a control framework is proposed which allows the control of an arbitrary number of Degrees of Freedom （DOF） through a single electromyogram （EMG） control input. Initially, the joint motions of nine test subjects were recorded while grasping and catching a cylinder. Inherent differences emerged depending upon whether the cylinder was grasped or caught. These data were used to form a distinct synergy for each task, described as the families of parametric functions of time that share a mutual time vector. These two Temporally Synchronized Synergies （TSS） were derived to reflect the task dependent control strategies adopted by the initial participants. These synergies were then mapped to a dexterous artificial hand that was subsequently controlled by two subjects with transradial amputations. The EMG signals from these subjects were used to replace the time vector shared by the synergies, enabling the subjects to perform both tasks with a dexterous artificial hand using only a single EMG input. After a ten minute training period, the subjects learned to use the dexterous artificial hand to grasp and catch the cylinder with 100.0% and 65.0% average success rates, respectively.     

Characterization of secretory proteins from cultured cauda epididymal cells that significantly sustain bovine sperm motility in vitro

Epididymis provides a safe environment in which stored-spermatozoa could survive for days before ejaculation. In vitro studies suggested that epididymal proteins seem to be implicated in sperm survival during coincubation with cultured epididymal cells. This study was basically designed to confirm if secretory proteins from bovine epididymal cell cultures provide sperm protection against rapid loss of sperm motility in vitro. Bovine spermatozoa were incubated in conditioned media (CM), which were prepared from cultured cauda epididymal cell (CEC). Motion parameters were recorded using a computer-assisted sperm analyzer. Sperm-free protein extracts from CM were fractionated by ultrafiltration through a 10-kDa cut off membrane. A significantly positive effect on sperm motility was observed when spermatozoa were incubated in CM (54 +/- 4%) and CM > 10 kDa (57 +/- 4%) compared to CM < 10-kDa fraction (30 +/- 3%) or fresh media (34 +/- 3%), after a 6-hr incubation period. This beneficial effect on sperm motility was abolished when the CM > 10-kDa fraction was heat-treated at 100 degrees C for 10 min. The CM > 10 kDa fraction provides factors that remained active even though spermatozoa were washed twice after a 2-hr preincubation period. To identify potential beneficial factors, bovine spermatozoa were incubated with radiolabeled proteins obtained using (35)S-methionine in culture medium. SDS-PAGE analysis of proteins extracted from CM-preincubated spermatozoa revealed the presence of a 42-kDa protein strongly associated to the sperm surface. This 42-kDa spot was trypsin-digested and identified by matrix-assisted laser desorption ionization-time of flight (MALDI-TOF) as a protein homologue to a 35-kDa bovine estrogen-sulfotransferase. This protein can play a role in epididymal biology and sperm function. Taken together, these results suggest that specific epididymal proteins can be implicated in the sperm protection in vitro, and can be characterized in our cell culture system.     

Effects of Visual Cues of Object Density on Perception and Anticipatory Control of Dexterous Manipulation

Anticipatory force planning during grasping is based on visual cues about the object’s physical properties and sensorimotor memories of previous actions with grasped objects. Vision can be used to estimate object mass based on the object size to identify and recall sensorimotor memories of previously manipulated objects. It is not known whether subjects can use density cues to identify the object’s center of mass (CM) and create compensatory moments in an anticipatory fashion during initial object lifts to prevent tilt. We asked subjects (n = 8) to estimate CM location of visually symmetric objects of uniform densities (plastic or brass, symmetric CM) and non-uniform densities (mixture of plastic and brass, asymmetric CM). We then asked whether subjects can use density cues to scale fingertip forces when lifting the visually symmetric objects of uniform and non-uniform densities. Subjects were able to accurately estimate an object’s center of mass based on visual density cues. When the mass distribution was uniform, subjects could scale their fingertip forces in an anticipatory fashion based on the estimation. However, despite their ability to explicitly estimate CM location when object density was non-uniform, subjects were unable to scale their fingertip forces to create a compensatory moment and prevent tilt on initial lifts. Hefting object parts in the hand before the experiment did not affect this ability. This suggests a dichotomy between the ability to accurately identify the object’s CM location for objects with non-uniform density cues and the ability to utilize this information to correctly scale their fingertip forces. These results are discussed in the context of possible neural mechanisms underlying sensorimotor integration linking visual cues and anticipatory control of grasping.     

Artificial gravity with ergometric exercise preserves the cardiac, but not cerebrovascular, functions during 4 days of head-down bed rest

Cardiovascular and musculoskeletal deconditioning occurring in long-term spaceflight requires new strategies to counteract these adverse effects. We previously reported that a short-arm centrifuge produced artificial gravity (AG), together with ergometer, has an approving effect on promoting cardiovascular function. The current study sought to investigate whether the cardiac and cerebrovascular functions were maintained and improved using a strategy of AG combined with exercise training on cardiovascular function during 4-day head-down bed rest (HDBR). Twelve healthy male subjects were assigned to a control group (CONT, n=6) and an AG combined with ergometric exercise training group (CM, n=6). Simultaneously, cardiac pumping and systolic functions, cerebral blood flow were measured before, during, and after HDBR. The results showed that AG combined with ergometric exercise caused an increase trend of number of tolerance, however, there was no significant difference between the two groups. After 4-day HDBR in the CONT group, heart rate increased significantly (59±6 vs 66±7 beats/min), while stroke volume (98±12 vs 68±13 mL) and cardiac output (6±1 vs 4±1 L/min) decreased significantly (p<0.05). All subjects had similar drops on cerebral vascular function. Volume regulating hormone aldosterone increased in both groups (by 119.9% in CONT group and 112.8% in the CM group), but only in the CONT group there were a significant changes (p<0.05). Angiotensin II was significantly increased by 140.5% after 4-day HDBR in the CONT group (p<0.05), while no significant changes were observed in the CM group. These results indicated that artificial gravity with ergometric exercise successfully eliminated changes induced by simulated weightlessness in heart rate, volume regulating hormones, and cardiac pumping function and partially maintained cardiac systolic function. Hence, a daily 1h alternating +1.0 and +2.0 Gz with 40 W exercise training appear to be an effective countermeasure against cardiac deconditioning.     

Muscle recruitment and coordination with an ankle exoskeleton

Exoskeletons have the potential to assist and augment human performance. Understanding how users adapt their movement and neuromuscular control in response to external assistance is important to inform the design of these devices. The aim of this research was to evaluate changes in muscle recruitment and coordination for ten unimpaired individuals walking with an ankle exoskeleton. We evaluated changes in the activity of individual muscles, cocontraction levels, and synergistic patterns of muscle coordination with increasing exoskeleton work and torque. Participants were able to selectively reduce activity of the ankle plantarflexors with increasing exoskeleton assistance. Increasing exoskeleton net work resulted in greater reductions in muscle activity than increasing exoskeleton torque. Patterns of muscle coordination were not restricted or constrained to synergistic patterns observed during unassisted walking. While three synergies could describe nearly 95% of the variance in electromyography data during unassisted walking, these same synergies could describe only 85–90% of the variance in muscle activity while walking with the exoskeleton. Synergies calculated with the exoskeleton demonstrated greater changes in synergy weights with increasing exoskeleton work versus greater changes in synergy activations with increasing exoskeleton torque. These results support the theory that unimpaired individuals do not exclusively use central pattern generators or other low-level building blocks to coordinate muscle activity, especially when learning a new task or adapting to external assistance, and demonstrate the potential for using exoskeletons to modulate muscle recruitment and coordination patterns for rehabilitation or performance.