Neural correlates of an illusionary sense of agency caused by virtual reality.

Sense of agency (SoA) is the sensation that self-actions lead to ensuing perceptual consequences. The prospective mechanism emphasizes that SoA arises from motor prediction and its comparison with actual action outcomes, while the reconstructive mechanism stresses that SoA emerges from retrospective causal processing about the action outcomes. Consistent with the prospective mechanism, motor planning regions were identified by neuroimaging studies using the temporal binding (TB) effect, a behavioral measure often linked to implicit SoA. Yet, TB also occurs during passive observation of another's action, lending support to the reconstructive mechanism, but its neural correlates remain unexplored. Here, we employed virtual reality (VR) to modulate such observation-based SoA and examined it with functional magnetic resonance imaging (fMRI). After manipulating an avatar hand in VR, participants passively observed an avatar's "action" and showed a significant increase in TB. The binding effect was associated with the right angular gyrus and inferior parietal lobule, which are critical nodes for inferential and agency processing. These results suggest that the experience of controlling an avatar may potentiate inferential processing within the right inferior parietal cortex and give rise to the illusionary SoA without voluntary action.

Gravity matters for the neural representations of action semantics.

The dynamic relationship between the neural representation of action word semantics and specific sensorimotor experience remains controversial. Here, we temporarily altered human subjects' sensorimotor experience in a 15-day head-down tilt bed rest setting, a ground-based analog of microgravity that disproportionally affects sensorimotor experiences of the lower limbs, and examined whether such effector-dependent activity deprivation specifically affected the neural processes of comprehending verbs of lower-limb actions (e.g. to kick) relative to upper-limb ones (e.g. to pinch). Using functional magnetic resonance imaging, we compared the multivoxel neural patterns for such action words prior to and after bed rest. We found an effector-specific (lower vs. upper limb) experience modulation in subcortical sensorimotor-related and anterior temporal regions. The neural action semantic representations in other effector-specific verb semantic regions (e.g. left lateral posterior temporal cortex) and motor execution regions were robust against such experience alterations. These effector-specific, sensorimotor-experience-sensitive and experience-independent patterns of verb neural representation highlight the multidimensional and dynamic nature of semantic neural representation, and the broad influence of microgravity (hence gravity) environment on cognition.

Pupil-Linked Arousal Response Reveals Aberrant Attention Regulation among Children with Autism Spectrum Disorder.

Autism spectrum disorder (ASD) is a developmental disorder that is characterized by difficulties with social interaction and interpersonal communication. It has been argued that abnormal attentional function to exogenous stimuli precedes and contributes to the core ASD symptoms. Notably, the locus ceruleus (LC) and its noradrenergic projections throughout the brain modulate attentional function, but the extent to which this locus ceruleus-norepinephrine (LC-NE) system influences attention in individuals with ASD, who frequently exhibit dysregulated alerting and attention orienting, is unknown. We examined dynamic attention control in girls and boys with ASD at rest using the pupil dilation response (PDR) as a noninvasive measure of LC-NE activity. When gender- and age-matched neurotypical participants were passively exposed to an auditory stream, their PDR decreased for recurrent stimuli but remained sensitive to surprising deviant stimuli. In contrast, children with ASD showed less habituation to recurrent stimuli as well as a diminished phasic response to deviants, particularly those containing social information. Their tonic habituation impairment predicts their phasic orienting impairment, and both impairments correlated with the severity of ASD symptom. Because of the fact that these pupil-linked responses are observed when individuals passively listen without any task engagement, our findings imply that the intricate and dynamic attention allocation mechanism, mediated by the subcortical LC-NE system, is impaired in ASD.SIGNIFICANCE STATEMENT Autistic individuals show attentional abnormalities to even simple sensory inputs, which emerge even before formal diagnosis. One possible mechanism behind these abnormalities is a malfunctioning pacemaker of their attention system, the locus ceruleus-norepinephrine pathway. Here we found, according to the pupillary response (a noradrenergic activity proxy), autistic children are hypersensitive to repeated sounds but hyposensitive to surprising deviant sounds when compared with age-matched controls. Importantly, hypersensitivity to repetitions predicts hyposensitivity to deviant sounds, and both abnormalities positively correlate to the severity of autistic symptoms. This provides strong evidence that autistic children have faulty noradrenergic regulation, which might underly the attentional atypicalities previously evidenced in various cortical responses in autistic individuals.

Sensorimotor knowledge from task-irrelevant feedback contributes to motor learning.

Exposure to task-irrelevant feedback leads to perceptual learning, but its effect on motor learning has been understudied. Here, we asked human participants to reach a visual target with a hand-controlled cursor while observing another cursor moving independently in a different direction. Although the task-irrelevant feedback did not change the main task's performance, it elicited robust savings in subsequent adaptation to classical visuomotor rotation perturbation. We demonstrated that the saving effect resulted from a faster formation of strategic learning through a series of experiments, not from gains in the implicit learning process. Furthermore, the saving effect was robust against drastic changes in stimulus features (i.e., rotation size or direction) or task types (i.e., for motor adaptation and skill learning). However, the effect was absent when the task-irrelevant feedback did not carry the visuomotor relationship embedded in visuomotor rotation. Thus, though previous research on perceptual learning has related task-irrelevant feedback to changes in early sensory processes, our findings support its role in acquiring abstract sensorimotor knowledge during motor learning. Motor learning studies have traditionally focused on task-relevant feedback, but our study extends the scope of feedback processes and sheds new light on the dichotomy of explicit and implicit learning in motor adaptation and motor structure learning.NEW & NOTEWORTHY When the motor system faces perturbations, such as fatigue or new environmental changes, it adapts to these changes by voluntarily selecting new action plans or implicitly fine-tuning the control. We show that the action selection part can be enhanced without practice or explicit instruction. We further demonstrate that this enhancement is probably linked to the acquisition of abstract knowledge about the to-be-adapted novel visual feedback. Our findings draw an interesting parallel between motor and perceptual learning by showing that top-down information affects both types of procedural learning.

Improving postural stability among people with lower-limb amputations by tactile sensory substitution.

BACKGROUND: For people with lower-limb amputations, wearing a prosthetic limb helps restore their motor abilities for daily activities. However, the prosthesis's potential benefits are hindered by limited somatosensory feedback from the affected limb and its prosthesis. Previous studies have examined various sensory substitution systems to alleviate this problem; the prominent approach is to convert foot-ground interaction to tactile stimulations. However, positive outcomes for improving their postural stability are still rare. We hypothesized that the sensory substiution system based on surrogated tactile stimulus is capable of improving the standing stability among people with lower-limb amputations. METHODS: We designed a wearable device consisting of four pressure sensors and two vibrators and tested it among people with unilateral transtibial amputations (n = 7) and non-disabled participants (n = 8). The real-time measurements of foot pressure were fused into a single representation of foot-ground interaction force, which was encoded by varying vibration intensity of the two vibrators attached to the participants' forearm. The vibration intensity followed a logarithmic function of the force representation, in keeping with principles of tactile psychophysics. The participants were tested with a classical postural stability task in which visual disturbances perturbed their quiet standing. RESULTS: With a brief familiarization of the system, the participants exhibited better postural stability against visual disturbances when switching on sensory substitution than without. The body sway was substantially reduced, as shown in head movements and excursions of the center of pressure. The improvement was present for both groups of participants and was particularly pronounced in more challenging conditions with larger visual disturbances. CONCLUSIONS: Substituting otherwise missing foot pressure feedback with vibrotactile signals can improve postural stability for people with lower-limb amputations. The design of the mapping between the foot-ground interaction force and the tactile signals is essential for the user to utilize the surrogated tactile signals for postural control, especially for situations that their postural control is challenged.

Savings in sensorimotor adaptation without an explicit strategy.

The hallmark of long-term retention of sensorimotor adaptation is a faster relearning when similar perturbations are encountered again. However, what processes underlie this saving effect is in debate. Though motor adaptation is traditionally viewed as a type of procedural learning, its savings has been recently shown to be solely based on a quick recall of explicit adaptation strategy. Here, we showed that adaptation to a novel error-invariant perturbation without an explicit strategy could enable subsequent savings. We further showed that adaptation to gradual perturbations could enable savings, which was supported by enhanced implicit learning. Our study provides supporting evidence that long-term retention of motor adaptation is possible without forming or recalling a cognitive strategy, and the interplay between implicit and explicit learning critically depends on the specifics of learning protocol and available sensory feedback.NEW & NOTEWORTHY Savings in motor learning sometimes refers to faster learning when one encounters the same perturbation again. Previous studies assert that forming a cognitive strategy for countering perturbations is necessary for savings. We used novel experimental techniques to prevent the formation of a cognitive strategy during initial adaptation and found that savings still existed during relearning. Our findings suggest that savings in sensorimotor adaptation do not exclusively depend on forming and recalling an explicit strategy.

Target selection by gaze pointing and manual confirmation: performance improved by locking the gaze cursor.

Eye movement-based human-computer interactions are emerging in diverse scenarios. When selecting targets on a user interface, the method of combining fast gaze pointing with reliable manual action is becoming increasingly popular. However, this method suffers from noise in gaze pointing caused by eye jitters and users' habitual early move-away of gaze before manual actions. Here we propose a novel solution to mitigate these problems by locking the gaze cursor at the target for imminent manual selection. We compared this gaze-lock cursor with a conventional gaze cursor in a typing task with varying key sizes and key gaps. Results show that typing performance was significantly better with larger key size and gap. More importantly, the gaze-lock cursor significantly increased speed and decreased errors when compared to a conventional gaze cursor. Our findings demonstrate that the gaze-lock cursor is a promising tool for gaze interactions involving frequent target selections. Practitioner summary: Target selection by gaze pointing and manual confirmation suffers from eye jitters and users' habitual early move-away of gaze before manual actions. The performance of this method can be improved by applying the gaze-lock cursor we proposed, increasing target size or increasing the target gap. Abbreviations: WTC: warping to target center; ALCM: automatic lock of cursor movement; LCD: liquid crystal display; EWMA: exponential weighted moving average; ER: error rate; ET: execution time; ED: edit distance; CV: coefficients of variation; ANOVA: analysis of variance; GUIs: general user interfaces.

Sensorimotor priors are effector dependent.

During sensorimotor tasks, subjects use sensory feedback but also prior information. It is often assumed that the sensorimotor prior is just given by the experiment and that the details for acquiring this prior (e.g., the effector) are irrelevant. However, recent research has suggested that the construction of priors is nontrivial. To test if the sensorimotor details matter for the construction of a prior, we designed two tasks that differ only in the effectors that subjects use to indicate their estimate. For both a typical reaching setting and an atypical wrist rotation setting, prior and feedback uncertainty matter as quantitatively predicted by Bayesian statistics. However, in violation of simple Bayesian models, the importance of the prior differs across effectors. Subjects overly rely on their prior in the typical reaching case compared with the wrist case. The brain is not naively Bayesian with a single and veridical prior. NEW & NOTEWORTHY Traditional Bayesian models often assume that we learn statistics of movements and use the information as a prior to guide subsequent movements. The effector is merely a reporting modality for information processing. We asked subjects to perform a visuomotor learning task with different effectors (finger or wrist). Surprisingly, we found that prior information is used differently between the effectors, suggesting that learning of the prior is related to the movement context such as the effector involved or that naive models of Bayesian behavior need to be extended.

Visuomotor learning is dependent on direction-specific error saliency.

People perceive better in cardinal directions compared with oblique ones. This directional effect, called oblique effect, has been documented in perception studies for a long time. However, typical motor studies do not differentiate learning in different directions. In this study we identify a significant directional effect in motor learning using visuomotor rotation paradigms. We find that adaptation to visual perturbations yields more savings when both initial learning and relearning are performed in cardinal directions than in oblique directions. We hypothesize that this directional effect arises from relatively higher error saliency in cardinal directions. Consistent with this hypothesis, we successfully increased savings in the oblique directions, which showed no saving effect before, by enhancing the error saliency with augmented visual feedback during learning. Our findings suggest that movement direction plays an important role in motor learning, especially when learning signals are direction specific. Our results also provide new insights about the role of motor errors in the formation and retrieval of motor memory and practical implications for promoting learning in motor rehabilitation and athletic training. NEW & NOTEWORTHY People perceive better when the stimulus is in cardinal directions than in oblique directions. Whether a similar directional effect exists in motor learning is unknown. Using a motor learning paradigm, we show that people relearn to compensate for a previously encountered perturbation faster when they move in cardinal directions than when they move in oblique directions. Further experimentation supports that this motor directional effect likely results from better sensory saliency of motor errors in cardinal directions.

What affects gait performance during walking while texting? A comparison of motor, visual and cognitive factors.

Texting on a cell phone disrupts walkers' gait performance. The performance decrement has been attributed to increased motor demand, decreased visual information and increased cognitive load. However, relative contributions of motor, visual and cognitive factors are poorly understood. Here we quantitatively estimated the relative contributions of these factors by comparing multiple walking conditions. Thirty-two adults walked for 20 m, with or without a dual task on the phone. The dual task was either a cognitively demanding digit ordering task or a casual tapping task. Gait performance was assessed using gait speed, stride length, stride time and stride time variability. Results showed that texting negatively impacted gait performance. Importantly, we found that cognitive factor contributed the most, visual factor the least, and motor factor in between. Our findings resolve the inconsistency in the literature and unambiguously show that motor, visual and cognitive factors caused by simultaneous phone use all contribute to gait alterations. Practitioner Summary: Walking performance is typically worsened when a concurrent phone use task such as texting is performed. We found that visual, motor and cognitive factors contributed to this performance decrement with increasing importance. Besides resolving inconsistency among previous reports, we also raised theoretical and practical concerns for phone use during walking.

Eliminating Direction Specificity in Visuomotor Learning.

The generalization of learning offers a unique window for investigating the nature of motor learning. Error-based motor learning reportedly cannot generalize to distant directions because the aftereffects are direction specific. This direction specificity is often regarded as evidence that motor adaptation is model-based learning, and is constrained by neuronal tuning characteristics in the primary motor cortices and the cerebellum. However, recent evidence indicates that motor adaptation also involves model-free learning and explicit strategy learning. Using rotation paradigms, here we demonstrate that savings (faster relearning), which is closely related to model-free learning and explicit strategy learning, is also direction specific. However, this new direction specificity can be abolished when the participants receive exposure to the generalization directions via an irrelevant visuomotor gain-learning task. Control evidence indicates that this exposure effect is weakened when direction error signals are absent during gain learning. Therefore, the direction specificity in visuomotor learning is not solely related to model-based learning; it may also result from the impeded expression of model-free learning and explicit strategy learning with untrained directions. Our findings provide new insights into the mechanisms underlying motor learning, and may have important implications for practical applications such as motor rehabilitation. SIGNIFICANCE STATEMENT: Motor learning is more useful if it generalizes to untrained scenarios when needed, especially for sports training and motor rehabilitation. However, as a form of motor learning, motor adaptation is typically direction specific. Here we first show that savings with motor adaptation, an index for model-free learning and explicit strategy learning in motor learning, is also direction specific. However, the participants' additional exposure to untrained directions via an irrelevant gain-learning task can enable the complete generalization of learning. Our findings challenge existing models of motor generalization and may have important implications for practical applications.

The Statistical Determinants of the Speed of Motor Learning.

It has recently been suggested that movement variability directly increases the speed of motor learning. Here we use computational modeling of motor adaptation to show that variability can have a broad range of effects on learning, both negative and positive. Experimentally, we also find contributing and decelerating effects. Lastly, through a meta-analysis of published papers, we verify that across a wide range of experiments, movement variability has no statistical relation with learning rate. While motor learning is a complex process that can be modeled, further research is needed to understand the relative importance of the involved factors.

Serotonin affects movement gain control in the spinal cord.

A fundamental challenge for the nervous system is to encode signals spanning many orders of magnitude with neurons of limited bandwidth. To meet this challenge, perceptual systems use gain control. However, whether the motor system uses an analogous mechanism is essentially unknown. Neuromodulators, such as serotonin, are prime candidates for gain control signals during force production. Serotonergic neurons project diffusely to motor pools, and, therefore, force production by one muscle should change the gain of others. Here we present behavioral and pharmaceutical evidence that serotonin modulates the input-output gain of motoneurons in humans. By selectively changing the efficacy of serotonin with drugs, we systematically modulated the amplitude of spinal reflexes. More importantly, force production in different limbs interacts systematically, as predicted by a spinal gain control mechanism. Psychophysics and pharmacology suggest that the motor system adopts gain control mechanisms, and serotonin is a primary driver for their implementation in force production.

Interference from mere thinking: mental rehearsal temporarily disrupts recall of motor memory.

Interference between successively learned tasks is widely investigated to study motor memory. However, how simultaneously learned motor memories interact with each other has been rarely studied despite its prevalence in daily life. Assuming that motor memory shares common neural mechanisms with declarative memory system, we made unintuitive predictions that mental rehearsal, as opposed to further practice, of one motor memory will temporarily impair the recall of another simultaneously learned memory. Subjects simultaneously learned two sensorimotor tasks, i.e., visuomotor rotation and gain. They retrieved one memory by either practice or mental rehearsal and then had their memory evaluated. We found that mental rehearsal, instead of execution, impaired the recall of unretrieved memory. This impairment was content-independent, i.e., retrieving either gain or rotation impaired the other memory. Hence, conscious recollection of one motor memory interferes with the recall of another memory. This is analogous to retrieval-induced forgetting in declarative memory, suggesting a common neural process across memory systems. Our findings indicate that motor imagery is sufficient to induce interference between motor memories. Mental rehearsal, currently widely regarded as beneficial for motor performance, negatively affects memory recall when it is exercised for a subset of memorized items.

Comparative assessment of surgeons' task performance and surgical ergonomics associated with conventional and modified flank positions: a simulation study.

BACKGROUND: Flank position is extensively used in retroperitoneoscopic urological practice. Most surgeons follow the patients' position in open approaches. However, surgical ergonomics of the conventional position in the retroperitoneoscopic surgery is poor. We introduce a modified position and evaluated task performance and surgical ergonomics of both positions with simulated surgical tasks. METHODS: Twenty-one novice surgeons were recruited to perform four tasks: bead transfer, ring transfer, continuous suturing, and cutting a circle. The conventional position was simulated by setting an endo-surgical simulator parallel to the long axis of a surgical desk. The modified position was simulated by rotating the simulator 30° with respect to the long axis of the desk. The outcome measurements include task performance measures, kinematic measures for body alignment, surface electromyography, relative loading between feet, and subjective ratings of fatigue. RESULTS: We observed significant improvements in both task performance and surgical ergonomics parameters under the modified position. For all four tasks, subjects finished tasks faster with higher accuracy (p < 0.005 or < 0.001). For ergonomics part: (1) The angle between the upper body and the head was decreased by 7.4 ± 1.7°; (2) The EMG amplitude collected from shoulders and left lumber was significantly lower (p < 0.05); (3) Relative loading between feet was more balanced (p < 0.001); (4) Manual-action muscles and postural muscles are rated less fatiguing according to the questionnaire (p < 0.05). CONCLUSIONS: Conventional position of patient in retroperitoneoscopic upper urinary tract surgery is associated with poor surgical ergonomics. With a simulated surgery, we demonstrated that our modified position could significantly improve task performance and surgical ergonomics. Further studies are still warranted to validate these benefits for both patients and surgeons.

Perceptual error based on Bayesian cue combination drives implicit motor adaptation.

The sensorimotor system can recalibrate itself without our conscious awareness, a type of procedural learning whose computational mechanism remains undefined. Recent findings on implicit motor adaptation, such as over-learning from small perturbations and fast saturation for increasing perturbation size, challenge existing theories based on sensory errors. We argue that perceptual error, arising from the optimal combination of movement-related cues, is the primary driver of implicit adaptation. Central to our theory is the increasing sensory uncertainty of visual cues with increasing perturbations, which was validated through perceptual psychophysics (Experiment 1). Our theory predicts the learning dynamics of implicit adaptation across a spectrum of perturbation sizes on a trial-by-trial basis (Experiment 2). It explains proprioception changes and their relation to visual perturbation (Experiment 3). By modulating visual uncertainty in perturbation, we induced unique adaptation responses in line with our model predictions (Experiment 4). Overall, our perceptual error framework outperforms existing models based on sensory errors, suggesting that perceptual error in locating one's effector, supported by Bayesian cue integration, underpins the sensorimotor system's implicit adaptation.

Abnormalities in motor adaptation to different types of perturbations in schizophreniaperturbations in schizophrenia.

Schizophrenia is a mental health disorder that often includes psychomotor disturbances, impacting how individuals adjust their motor output based on the cause of motor errors. While previous motor adaptation studies on individuals with schizophrenia have largely focused on large and consistent perturbations induced by abrupt experimental manipulations, such as donning prism goggles, the adaptation process to random perturbations, either caused by intrinsic motor noise or external disturbances, has not been examined - despite its ecological relevance. Here, we used a unified behavioral task paradigm to examine motor adaptation to perturbations of three causal structures among individuals in the remission stage of schizophrenia, youth with ultra-high risk of psychosis, adults with active symptoms, and age-matched controls. Results showed that individuals with schizophrenia had reduced trial-by-trial adaptation and large error variance when adapting to their own motor noise. When adapting to random but salient perturbations, they showed intact adaptation and normal causal inference of errors. This contrasted with reduced adaptation to large yet consistent perturbations, which could reflect difficulties in forming cognitive strategies rather than the often-assumed impairments in procedural learning or sense of agency. Furthermore, the observed adaptation effects were correlated with the severity of positive symptoms across the diagnosis groups. Our findings suggest that individuals with schizophrenia face challenges in accommodating intrinsic perturbations when motor errors are ambiguous but adapt with intact causal attribution when errors are salient.

Generalization of unconstrained reaching with hand-weight changes.

Studies of motor generalization usually perturb hand reaches by distorting visual feedback with virtual reality or by applying forces with a robotic manipulandum. Whereas such perturbations are useful for studying how the central nervous system adapts and generalizes to novel dynamics, they are rarely encountered in daily life. The most common perturbations that we experience are changes in the weights of objects that we hold. Here, we use a center-out, free-reaching task, in which we can manipulate the weight of a participant's hand to examine adaptation and generalization following naturalistic perturbations. In both trial-by-trial paradigms and block-based paradigms, we find that learning converges rapidly (on a timescale of approximately two trials), and this learning generalizes mostly to movements in nearby directions with a unimodal pattern. However, contrary to studies using more artificial perturbations, we find that the generalization has a strong global component. Furthermore, the generalization is enhanced with repeated exposure of the same perturbation. These results suggest that the familiarity of a perturbation is a major factor in movement generalization and that several theories of the neural control of movement, based on perturbations applied by robots or in virtual reality, may need to be extended by incorporating prior influence that is characterized by the familiarity of the perturbation.

Lower limb wearable capacitive sensing and its applications to recognizing human gaits.

In this paper, we present an approach to sense human body capacitance and apply it to recognize lower limb locomotion modes. The proposed wearable sensing system includes sensing bands, a signal processing circuit and a gait event detection module. Experiments on long-term working stability, adaptability to disturbance and locomotion mode recognition are carried out to validate the effectiveness of the proposed approach. Twelve able-bodied subjects are recruited, and eleven normal gait modes are investigated. With an event-dependent linear discriminant analysis classifier and feature selection procedure, four time-domain features are used for pattern recognition and satisfactory recognition accuracies (97:3% ± 0:5%, 97:0% ± 0:4%, 95:6% ± 0:9% and 97:0% ± 0:4% for four phases of one gait cycle respectively) are obtained. The accuracies are comparable with that from electromyography-based systems and inertial-based systems. The results validate the effectiveness of the proposed lower limb capacitive sensing approach in recognizing human normal gaits.

Atypical development of social and nonsocial working memory capacity among preschoolers with autism spectrum disorders.

Individuals with autism spectrum disorders (ASD) have shown impaired performance in canonical and nonsocial working memory (WM). However, no study has investigated social WM and its early development. Using biological motion stimuli, our study assessed the development of social and nonsocial WM capacity among children with or without ASD across the age span between 4 and 6 (N = 150). While typically developing (TD) children show a rapid development from age 5 to 6, children with ASD showed a delayed development for both social and nonsocial WM capacity, reaching a significant group difference at age 6. Furthermore, we found a negative correlation between social (but not nonsocial) WM capacity and the severity of autistic symptoms among children with ASD. In contrast, there is a positive correlation between both types of WM capacity and intelligence among TD children but not among children with ASD. Our findings thus indicate that individuals with ASD miss the rapid development of WM capacity in early childhood and, particularly, their delayed social WM development might contribute to core symptoms that critically depend on social information processing.