The relativity of reaching: Motion of the touched surface alters the trajectory of hand movements.

For dexterous control of the hand, humans integrate sensory information and prior knowledge regarding their bodies and the world. We studied the role of touch in hand motor control by challenging a fundamental prior assumption-that self-motion of inanimate objects is unlikely upon contact. In a reaching task, participants slid their fingertips across a robotic interface, with their hand hidden from sight. Unbeknownst to the participants, the robotic interface remained static, followed hand movement, or moved in opposition to it. We considered two hypotheses. Either participants were able to account for surface motion or, if the stationarity assumption held, they would integrate the biased tactile cues and proprioception. Motor errors consistent with the latter hypothesis were observed. The role of visual feedback, tactile sensitivity, and friction was also investigated. Our study carries profound implications for human-machine collaboration in a world where objects may no longer conform to the stationarity assumption.

Synaptic inputs to motor neurons underlying muscle coactivation for functionally different tasks have different spectral characteristics.

The central nervous system (CNS) may produce the same endpoint trajectory or torque profile with different muscle activation patterns. What differentiates these patterns is the presence of cocontraction, which does not contribute to effective torque generation but allows to modulate joints' mechanical stiffness. Although it has been suggested that the generation of force and the modulation of stiffness rely on separate pathways, a characterization of the differences between the synaptic inputs to motor neurons (MNs) underlying these tasks is still missing. In this study, participants coactivated the same pair of upper-limb muscles, i.e., the biceps brachii and the triceps brachii, to perform two functionally different tasks: limb stiffness modulation or endpoint force generation. Spike trains of MNs were identified through decomposition of high-density electromyograms (EMGs) collected from the two muscles. Cross-correlogram showed a higher synchronization between MNs recruited to modulate stiffness, whereas cross-muscle coherence analysis revealed peaks in the ß-band, which is commonly ascribed to a cortical origin. These peaks did not appear during the coactivation for force generation, thus suggesting separate cortical inputs for stiffness modulation. Moreover, a within-muscle coherence analysis identified two subsets of MNs that were selectively recruited to generate force or regulate stiffness. This study is the first to highlight different characteristics, and probable different neural origins, of the synaptic inputs driving a pair of muscles under different functional conditions. We suggest that stiffness modulation is driven by cortical inputs that project to a separate set of MNs, supporting the existence of a separate pathway underlying the control of stiffness.NEW & NOTEWORTHY The characterization of the pathways underlying force generation or stiffness modulation are still unknown. In this study, we demonstrated that the common input to motor neurons of antagonist muscles shows a high-frequency component when muscles are coactivated to modulate stiffness but not to generate force. Our results provide novel insights on the neural strategies for the recruitment of multiple muscles by identifying specific spectral characteristics of the synaptic inputs underlying functionally different tasks.

Interception of vertically approaching objects: temporal recruitment of the internal model of gravity and contribution of optical information.

Introduction: Recent views posit that precise control of the interceptive timing can be achieved by combining on-line processing of visual information with predictions based on prior experience. Indeed, for interception of free-falling objects under gravity's effects, experimental evidence shows that time-to-contact predictions can be derived from an internal gravity representation in the vestibular cortex. However, whether the internal gravity model is fully engaged at the target motion outset or reinforced by visual motion processing at later stages of motion is not yet clear. Moreover, there is no conclusive evidence about the relative contribution of internalized gravity and optical information in determining the time-to-contact estimates. Methods: We sought to gain insight on this issue by asking 32 participants to intercept free falling objects approaching directly from above in virtual reality. Object motion had durations comprised between 800 and 1100 ms and it could be either congruent with gravity (1 g accelerated motion) or not (constant velocity or -1 g decelerated motion). We analyzed accuracy and precision of the interceptive responses, and fitted them to Bayesian regression models, which included predictors related to the recruitment of a priori gravity information at different times during the target motion, as well as based on available optical information. Results: Consistent with the use of internalized gravity information, interception accuracy and precision were significantly higher with 1 g motion. Moreover, Bayesian regression indicated that interceptive responses were predicted very closely by assuming engagement of the gravity prior 450 ms after the motion onset, and that adding a predictor related to on-line processing of optical information improved only slightly the model predictive power. Discussion: Thus, engagement of a priori gravity information depended critically on the processing of the first 450 ms of visual motion information, exerting a predominant influence on the interceptive timing, compared to continuously available optical information. Finally, these results may support a parallel processing scheme for the control of interceptive timing.

A novel force-constrained non-negative matrix factorization algorithm reveals the effectiveness of muscle synergies in the task space.

According to the synergy hypothesis, the motor system recruits a small number of synergies in a task-dependent manner. Existing synergy extraction algorithms typically only consider the muscle pattern and it remains unclear to which extent muscle synergies encode task-relevant variations of muscle activity. We propose a novel force-constrained non-negative matrix algorithm (FCNMF) based on a gradient descent update rule that considers also the task space by adding a term penalizing force reconstruction error in the cost function. We validated the FCNMF algorithm using simulated muscle data and corrupted them by noise. We compared task performances with reconstructed trajectories using synergies (RS) extracted from the FCNMF algorithm and from the standard multiplicative non-negative matrix factorization NMF algorithm. We found that FCNMF outperforms NMF for different types of noise. Finally, we demonstrated the effectiveness of FCNMF on EMG data collected during an isometric reaching task. The new algorithm accurately reconstructs the trajectories in all participants, even in those for which the NMF algorithm fails. These findings show the effectiveness of muscle synergies extracted considering the task space, possibly thanks to the robustness of FCNMF against non-isotropic noise present in muscle data, suggesting that they provide an effective strategy for motor coordination.

Head-centric computing for vestibular stimulation under head-free conditions.

Background: The vestibular end organs (semicircular canals, saccule and utricle) monitor head orientation and motion. Vestibular stimulation by means of controlled translations, rotations or tilts of the head represents a routine manoeuvre to test the vestibular apparatus in a laboratory or clinical setting. In diagnostics, it is used to assess oculomotor postural or perceptual responses, whose abnormalities can reveal subclinical vestibular dysfunctions due to pathology, aging or drugs. Objective: The assessment of the vestibular function requires the alignment of the motion stimuli as close as possible with reference axes of the head, for instance the cardinal axes naso-occipital, interaural, cranio-caudal. This is often achieved by using a head restraint, such as a helmet or strap holding the head tightly in a predefined posture that guarantees the alignment described above. However, such restraints may be quite uncomfortable, especially for elderly or claustrophobic patients. Moreover, it might be desirable to test the vestibular function under the more natural conditions in which the head is free to move, as when subjects are tracking a visual target or they are standing erect on the moving platform. Here, we document algorithms that allow delivering motion stimuli aligned with head-fixed axes under head-free conditions. Methods: We implemented and validated these algorithms using a MOOG-6DOF motion platform in two different conditions. 1) The participant kept the head in a resting, fully unrestrained posture, while inter-aural, naso-occipital or cranio-caudal translations were applied. 2) The participant moved the head continuously while a naso-occipital translation was applied. Head and platform motion were monitored in real-time using Vicon. Results: The results for both conditions showed excellent agreement between the theoretical spatio-temporal profile of the motion stimuli and the corresponding profile of actual motion as measured in real-time. Conclusion: We propose our approach as a safe, non-intrusive method to test the vestibular system under the natural head-free conditions required by the experiential perspective of the patients.

Rhythmic tapping to a moving beat motion kinematics overrules natural gravity.

Beat induction is the cognitive ability that allows humans to listen to a regular pulse in music and move in synchrony with it. Although auditory rhythmic cues induce more consistent synchronization than flashing visual metronomes, this auditory-visual asymmetry can be canceled by visual moving stimuli. Here, we investigated whether the naturalness of visual motion or its kinematics could provide a synchronization advantage over flashing metronomes. Subjects were asked to tap in sync with visual metronomes defined by vertically accelerating/decelerating motion, either congruent or not with natural gravity; horizontally accelerating/decelerating motion; or flashing stimuli. We found that motion kinematics was the predominant factor determining rhythm synchronization, as accelerating moving metronomes in any cardinal direction produced more precise and predictive tapping than decelerating or flashing conditions. Our results support the notion that accelerating visual metronomes convey a strong sense of beat, as seen in the cueing movements of an orchestra director.

Effect of age and speed on the step-to-step transition strategies in children.

The development and acquisition of mature walking in children is multifactorial, depending among others on foot interaction with the ground, body dynamics and the knowledge of the 'rules' stemming from the gravity field. Indeed, each step the velocity of the centre of mass must be redirected upwards. This redirection may be initiated by the trailing leg, propulsing forward and upward the body before foot contact, or later by the loading limb after the contact with the ground. While it has been suggested that mature walking develops slowly from first independent steps to about 7 years of age, it is still unknown how children acquire the appropriate loading and propulsion forces during the step-to-step transition. To answer that question, twenty-four children (from 3 to 12 years old) and twelve young adults (from 20 to 27 years old) walked on force platforms at different walking speed. The ground reaction forces under each foot were recorded and the vertical velocity of the centre of mass of the body was computed. With decreasing age and increasing velocity (or Froude number), the occurrence of unanticipated transition is higher, related to a different ratio between the vertical support of the front and back leg. The different transition strategy observed in children indicates that body weight transfer from one limb to the other is not fully mature at 12 years old.

Noise and vestibular perception of passive self-motion.

Noise defined as random disturbances is ubiquitous in both the external environment and the nervous system. Depending on the context, noise can degrade or improve information processing and performance. In all cases, it contributes to neural systems dynamics. We review some effects of various sources of noise on the neural processing of self-motion signals at different stages of the vestibular pathways and the resulting perceptual responses. Hair cells in the inner ear reduce the impact of noise by means of mechanical and neural filtering. Hair cells synapse on regular and irregular afferents. Variability of discharge (noise) is low in regular afferents and high in irregular units. The high variability of irregular units provides information about the envelope of naturalistic head motion stimuli. A subset of neurons in the vestibular nuclei and thalamus are optimally tuned to noisy motion stimuli that reproduce the statistics of naturalistic head movements. In the thalamus, variability of neural discharge increases with increasing motion amplitude but saturates at high amplitudes, accounting for behavioral violation of Weber's law. In general, the precision of individual vestibular neurons in encoding head motion is worse than the perceptual precision measured behaviorally. However, the global precision predicted by neural population codes matches the high behavioral precision. The latter is estimated by means of psychometric functions for detection or discrimination of whole-body displacements. Vestibular motion thresholds (inverse of precision) reflect the contribution of intrinsic and extrinsic noise to perception. Vestibular motion thresholds tend to deteriorate progressively after the age of 40 years, possibly due to oxidative stress resulting from high discharge rates and metabolic loads of vestibular afferents. In the elderly, vestibular thresholds correlate with postural stability: the higher the threshold, the greater is the postural imbalance and risk of falling. Experimental application of optimal levels of either galvanic noise or whole-body oscillations can ameliorate vestibular function with a mechanism reminiscent of stochastic resonance. Assessment of vestibular thresholds is diagnostic in several types of vestibulopathies, and vestibular stimulation might be useful in vestibular rehabilitation.

Muscle Activity during Passive and Active Movements in Preterm and Full-Term Infants.

Manifestation of muscle reactions at an early developmental stage may reflect the processes underlying the generation of appropriate muscle tone, which is also an integral part of all movements. In preterm infants, some aspects of muscular development may occur differently than in infants born at term. Here we evaluated early manifestations of muscle tone by measuring muscle responses to passive stretching (StR) and shortening (ShR) in both upper and lower limbs in preterm infants (at the corrected age from 0 weeks to 12 months), and compared them to those reported in our previous study on full-term infants. In a subgroup of participants, we also assessed spontaneous muscle activity during episodes of relatively large limb movements. The results showed very frequent StR and ShR, and also responses in muscles not being primarily stretched/shortened, in both preterm and full-term infants. A reduction of sensorimotor responses to muscle lengthening and shortening with age suggests a reduction in excitability and/or the acquisition of functionally appropriate muscle tone during the first year of life. The alterations of responses during passive and active movements in preterm infants were primarily seen in the early months, perhaps reflecting temporal changes in the excitability of the sensorimotor networks.

Comparison of the forward and sideways locomotor patterns in children with Cerebral Palsy.

Switching locomotion direction is a common task in daily life, and it has been studied extensively in healthy people. Little is known, however, about the locomotor adjustments involved in changing locomotion direction from forward (FW) to sideways (SW) in children with cerebral palsy (CP). The importance of testing the ability of children with CP in this task lies in the assessment of flexible, adaptable adjustments of locomotion as a function of the environmental context. On the one hand, the ability of a child to cope with novel task requirements may provide prognostic cues as to the chances of modifying the gait adaptively. On the other hand, challenging the child with the novel task may represent a useful rehabilitation tool to improve the locomotor performance. SW is an asymmetrical locomotor task and requires a differential control of right and left limb muscles. Here, we report the results of a cross-sectional study comparing FW and SW in 27 children with CP (17 diplegic, 10 hemiplegic, 2-10 years) and 18 age-matched typically developing (TD) children. We analyzed gait kinematics, joint moments, EMG activity of 12 pairs of bilateral muscles, and muscle modules evaluated by factorization of EMG signals. Task performance in several children with CP differed drastically from that of TD children. Only 2/3 of children with CP met the primary outcome, i.e. they succeeded to step sideways, and they often demonstrated attempts to step forward. They tended to rotate their trunk FW, cross one leg over the other, flex the knee and hip. Moreover, in contrast to TD children, children with CP often exhibited similar motor modules for FW and SW. Overall, the results reflect developmental deficits in the control of gait, bilateral coordination and adjustment of basic motor modules in children with CP. We suggest that the sideways (along with the backward) style of locomotion represents a novel rehabilitation protocol that challenges the child to cope with novel contextual requirements.

A case report of agoraphobia following right parietal lobe surgery: changes in functional and structural connectivities of the multimodal vestibular network.

Agoraphobia is a visuo-vestibular-spatial disorder that may involve dysfunction of the vestibular network, which includes the insular and limbic cortex. We sought to study the neural correlates of this disorder in an individual who developed agoraphobia after surgical removal of a high-grade glioma located in the right parietal lobe, by assessing pre- and post-surgery connectivities in the vestibular network. The patient underwent surgical resection of the glioma located within the right supramarginal gyrus. The resection interested also portions of the superior and inferior parietal lobe. Structural and functional connectivities were assessed through magnetic resonance imaging before and 5 and 7 months after surgery. Connectivity analyses focused on a network comprising 142 spherical regions of interest (4 mm radius) associated with the vestibular cortex: 77 in the left and 65 in the right hemisphere (excluding lesioned regions). Tractography for diffusion-weighted structural data and correlation between time series for functional resting-state data were calculated for each pair of regions in order to build weighted connectivity matrices. Graph theory was applied to assess post-surgery changes in network measures, such as strength, clustering coefficient, and local efficiency. Structural connectomes after surgery showed a decrease of strength in the preserved ventral portion of the supramarginal gyrus (PFcm) and in a high order visual motion area in the right middle temporal gyrus (37dl), and decrease of the clustering coefficient and of the local efficiency in several areas of the limbic, insular cortex, parietal and frontal cortex, indicating general disconnection of the vestibular network. Functional connectivity analysis showed both a decrease in connectivity metrics, mainly in high-order visual areas and in the parietal cortex, and an increase in connectivity metrics, mainly in the precuneus, parietal and frontal opercula, limbic, and insular cortex. This post-surgery reorganization of the vestibular network is compatible with altered processing of visuo-vestibular-spatial information, yielding agoraphobia symptoms. Specifically, post-surgical functional increases of clustering coefficient and local efficiency in the anterior insula and in the cingulate cortex might indicate a more predominant role of these areas within the vestibular network, which could be predictive of the fear and avoiding behavior characterizing agoraphobia.

Characterization of prosthetic knees through a low-dimensional description of gait kinematics.

The characterization of both limbs' behaviour in prosthetic gait is of key importance for improving the prosthetic components and increasing the biomechanical capability of trans-femoral amputees. When characterizing human gait, modular motor control theories have been proven to be powerful in providing a compact description of the gait patterns. In this paper, the planar covariation law of lower limb elevation angles is proposed as a compact, modular description of prosthetic gait; this model is exploited for a comparison between trans-femoral amputees walking with different prosthetic knees and control subjects walking at different speeds. Results show how the planar covariation law is maintained in prostheses users, with a similar spatial organization and few temporal differences. Most of the differences among the different prosthetic knees are found in the kinematic coordination patterns of the sound side. Moreover, different geometrical parameters have been calculated over the common projected plane, and their correlation with classical gait spatiotemporal and stability parameters has been investigated. The results from this latter analysis have highlighted a correlation with several parameters of gait, suggesting that this compact description of kinematics unravels a significant biomechanical meaning. These results can be exploited to guide the control mechanisms of prosthetic devices based purely on the measurement of relevant kinematic quantities.

Bayesian hierarchical models and prior elicitation for fitting psychometric functions.

Our previous articles demonstrated how to analyze psychophysical data from a group of participants using generalized linear mixed models (GLMM) and two-level methods. The aim of this article is to revisit hierarchical models in a Bayesian framework. Bayesian models have been previously discussed for the analysis of psychometric functions although this approach is still seldom applied. The main advantage of using Bayesian models is that if the prior is informative, the uncertainty of the parameters is reduced through the combination of prior knowledge and the experimental data. Here, we evaluate uncertainties between and within participants through posterior distributions. To demonstrate the Bayesian approach, we re-analyzed data from two of our previous studies on the tactile discrimination of speed. We considered different methods to include a priori knowledge in the prior distribution, not only from the literature but also from previous experiments. A special type of Bayesian model, the power prior distribution, allowed us to modulate the weight of the prior, constructed from a first set of data, and use it to fit a second one. Bayesian models estimated the probability distributions of the parameters of interest that convey information about the effects of the experimental variables, their uncertainty, and the reliability of individual participants. We implemented these models using the software Just Another Gibbs Sampler (JAGS) that we interfaced with R with the package rjags. The Bayesian hierarchical model will provide a promising and powerful method for the analysis of psychometric functions in psychophysical experiments.

Development of running is not related to time since onset of independent walking, a longitudinal case study.

Introduction: Children start to run after they master walking. How running develops, however, is largely unknown. Methods: We assessed the maturity of running pattern in two very young, typically developing children in a longitudinal design spanning about three years. Leg and trunk 3D kinematics and electromyography collected in six recording sessions, with more than a hundred strides each, entered our analysis. We recorded walking during the first session (the session of the first independent steps of the two toddlers at the age of 11.9 and 10.6 months) and fast walking or running for the subsequent sessions. More than 100 kinematic and neuromuscular parameters were determined for each session and stride. The equivalent data of five young adults served to define mature running. After dimensionality reduction using principal component analysis, hierarchical cluster analysis based on the average pairwise correlation distance to the adult running cluster served as a measure for maturity of the running pattern. Results: Both children developed running. Yet, in one of them the running pattern did not reach maturity whereas in the other it did. As expected, mature running appeared in later sessions (>13 months after the onset of independent walking). Interestingly, mature running alternated with episodes of immature running within sessions. Our clustering approach separated them. Discussion: An additional analysis of the accompanying muscle synergies revealed that the participant who did not reach mature running had more differences in muscle contraction when compared to adults than the other. One may speculate that this difference in muscle activity may have caused the difference in running pattern.

Enhancement of Vestibular Motion Discrimination by Small Stochastic Whole-body Perturbations in Young Healthy Humans.

Noisy galvanic vestibular stimulation has been shown to improve vestibular perception in healthy subjects. Here, we sought to obtain similar results using more natural stimuli consisting of small-amplitude motion perturbations of the whole body. Thirty participants were asked to report the perceived direction of antero-posterior sinusoidal motion on a MOOG platform. We compared the baseline perceptual thresholds with those obtained by applying small, stochastic perturbations at different power levels along the antero-posterior axis, symmetrically distributed around a zero-mean. At the population level, we found that the thresholds for all but the highest level of noise were significantly lower than the baseline threshold. At the individual level, the threshold was lower with at least one noise level than the threshold without noise in 87% of participants. Thus, small, stochastic oscillations of the whole body can increase the probability of recognizing the direction of motion from low, normally subthreshold vestibular signals, possibly due to stochastic resonance mechanisms. We suggest that, just as the external noise of the present experiments, also the spontaneous random oscillations of the head and body associated with standing posture are beneficial by enhancing vestibular thresholds with a mechanism similar to stochastic resonance.

Complexity of modular neuromuscular control increases and variability decreases during human locomotor development.

When does modular control of locomotion emerge during human development? One view is that modularity is not innate, being learnt over several months of experience. Alternatively, the basic motor modules are present at birth, but are subsequently reconfigured due to changing brain-body-environment interactions. One problem in identifying modular structures in stepping infants is the presence of noise. Here, using both simulated and experimental muscle activity data from stepping neonates, infants, preschoolers, and adults, we dissect the influence of noise, and identify modular structures in all individuals, including neonates. Complexity of modularity increases from the neonatal stage to adulthood at multiple levels of the motor infrastructure, from the intrinsic rhythmicity measured at the level of individual muscles activities, to the level of muscle synergies and of bilateral intermuscular network connectivity. Low complexity and high variability of neuromuscular signals attest neonatal immaturity, but they also involve potential benefits for learning locomotor tasks.

Interception of virtual throws reveals predictive skills based on the visual processing of throwing kinematics.

Predicting the outcome of observed actions is fundamental for efficient interpersonal interactions. This is evident in interceptive sports, where predicting the future ball trajectory could make apart success and fail. We quantitatively assessed the predictive abilities of non-trained adults intercepting thrown balls in immersive virtual reality. Participants performed better when they could see the complete throwing action in addition to the ball flight, and they were able to move toward the correct direction when the ball flight was occluded. In both cases, performance varies with the individual motor style of the thrower. These results prove that humans can effectively predict the unfolding of complex full-body actions, with no need to extensively practice them, and that such predictions are exploited online to optimize interactive motor performance. This suggests that humans hold a functional knowledge of how actions recurrent in the human motor repertoire map into the changes brought to the environment.

Characterizing the Gait of People With Different Types of Amputation and Prosthetic Components Through Multimodal Measurements: A Methodological Perspective.

Prosthetic gait implies the use of compensatory motor strategies, including alterations in gait biomechanics and adaptations in the neural control mechanisms adopted by the central nervous system. Despite the constant technological advancements in prostheses design that led to a reduction in compensatory movements and an increased acceptance by the users, a deep comprehension of the numerous factors that influence prosthetic gait is still needed. The quantitative prosthetic gait analysis is an essential step in the development of new and ergonomic devices and to optimize the rehabilitation therapies. Nevertheless, the assessment of prosthetic gait is still carried out by a heterogeneous variety of methodologies, and this limits the comparison of results from different studies, complicating the definition of shared and well-accepted guidelines among clinicians, therapists, physicians, and engineers. This perspective article starts from the results of a project funded by the Italian Worker's Compensation Authority (INAIL) that led to the generation of an extended dataset of measurements involving kinematic, kinetic, and electrophysiological recordings in subjects with different types of amputation and prosthetic components. By encompassing different studies published along the project activities, we discuss the specific information that can be extracted by different kinds of measurements, and we here provide a methodological perspective related to multimodal prosthetic gait assessment, highlighting how, for designing improved prostheses and more effective therapies for patients, it is of critical importance to analyze movement neural control and its mechanical actuation as a whole, without limiting the focus to one specific aspect.

Masking Vibrations and Contact Force Affect the Discrimination of Slip Motion Speed in Touch.

Multiple cues contribute to the discrimination of slip motion speed by touch. In our previous article, we demonstrated that masking vibrations at various frequencies impaired the discrimination of speed. In this article, we extended the previous results to evaluate this phenomenon on a smooth glass surface, and for different values of contact force and duration of the masking stimulus. Speed discrimination was significantly impaired by masking vibrations at high but not at low contact force. Furthermore, a short pulse of masking vibrations at motion onset produced a similar effect as the long masking stimulus, delivered throughout slip motion duration. This last result suggests that mechanical events at motion onset provide important cues to the discrimination of speed.