When and why does motor preparation arise in recurrent neural network models of motor control?

During delayed ballistic reaches, motor areas consistently display movement-specific activity patterns prior to movement onset. It is unclear why these patterns arise: while they have been proposed to seed an initial neural state from which the movement unfolds, recent experiments have uncovered the presence and necessity of ongoing inputs during movement, which may lessen the need for careful initialization. Here, we modeled the motor cortex as an input-driven dynamical system, and we asked what the optimal way to control this system to perform fast delayed reaches is. We find that delay-period inputs consistently arise in an optimally controlled model of M1. By studying a variety of network architectures, we could dissect and predict the situations in which it is beneficial for a network to prepare. Finally, we show that optimal input-driven control of neural dynamics gives rise to multiple phases of preparation during reach sequences, providing a novel explanation for experimentally observed features of monkey M1 activity in double reaching.

When preparation pays off.

Computational principles shed light on why movement is preceded by preparatory activity within the neural networks that control muscles.

A neural basis of choking under pressure.

Incentives tend to drive improvements in performance. But when incentives get too high, we can "choke under pressure" and underperform right when it matters most. What neural processes might lead to choking under pressure? We studied rhesus monkeys performing a challenging reaching task in which they underperformed when an unusually large "jackpot" reward was at stake, and we sought a neural mechanism that might result in that underperformance. We found that increases in reward drive neural activity during movement preparation into, and then past, a zone of optimal performance. We conclude that neural signals of reward and motor preparation interact in the motor cortex (MC) in a manner that can explain why we choke under pressure.

Optimality of multisensory integration while compensating for uncertain visual target information with artificial vibrotactile cues during reach planning.

BACKGROUND: Planning and executing movements requires the integration of different sensory modalities, such as vision and proprioception. However, neurological diseases like stroke can lead to full or partial loss of proprioception, resulting in impaired movements. Recent advances focused on providing additional sensory feedback to patients to compensate for the sensory loss, proving vibrotactile stimulation to be a viable option as it is inexpensive and easy to implement. Here, we test how such vibrotactile information can be integrated with visual signals to estimate the spatial location of a reach target. METHODS: We used a center-out reach paradigm with 31 healthy human participants to investigate how artificial vibrotactile stimulation can be integrated with visual-spatial cues indicating target location. Specifically, we provided multisite vibrotactile stimulation to the moving dominant arm using eccentric rotating mass (ERM) motors. As the integration of inputs across multiple sensory modalities becomes especially relevant when one of them is uncertain, we additionally modulated the reliability of visual cues. We then compared the weighing of vibrotactile and visual inputs as a function of visual uncertainty to predictions from the maximum likelihood estimation (MLE) framework to decide if participants achieve quasi-optimal integration. RESULTS: Our results show that participants could estimate target locations based on vibrotactile instructions. After short training, combined visual and vibrotactile cues led to higher hit rates and reduced reach errors when visual cues were uncertain. Additionally, we observed lower reaction times in trials with low visual uncertainty when vibrotactile stimulation was present. Using MLE predictions, we found that integration of vibrotactile and visual cues followed optimal integration when vibrotactile cues required the detection of one or two active motors. However, if estimating the location of a target required discriminating the intensities of two cues, integration violated MLE predictions. CONCLUSION: We conclude that participants can quickly learn to integrate visual and artificial vibrotactile information. Therefore, using additional vibrotactile stimulation may serve as a promising way to improve rehabilitation or the control of prosthetic devices by patients suffering loss of proprioception.

Novel comprehensive analysis of skilled reaching and grasping behavior in adult rats.

BACKGROUND: Reaching and grasping (R&G) in rats is commonly used as an outcome measure to investigate the effectiveness of rehabilitation or treatment strategies to recover forelimb function post spinal cord injury. Kinematic analysis has been limited to the wrist and digit movements. Kinematic profiles of the more proximal body segments that play an equally crucial role in successfully executing the task remain unexplored. Additionally, understanding of different forelimb muscle activity, their interactions, and their correlation with the kinematics of R&G movement is scarce. NEW METHOD: In this work, novel methodologies to comprehensively assess and quantify the 3D kinematics of the proximal and distal forelimb joints along with associated muscle activity during R&G movements in adult rats are developed and discussed. RESULTS: Our data show that different phases of R&G identified using the novel kinematic and EMG-based approach correlate with the well-established descriptors of R&G stages derived from the Whishaw scoring system. Additionally, the developed methodology allows describing the temporal activity of individual muscles and associated mechanical and physiological properties during different phases of the motor task. COMPARISON WITH EXISTING METHOD(S): R&G phases and their sub-components are identified and quantified using the developed kinematic and EMG-based approach. Importantly, the identified R&G phases closely match the well-established qualitative descriptors of the R&G task proposed by Whishaw and colleagues. CONCLUSIONS: The present work provides an in-depth objective analysis of kinematics and EMG activity of R&G behavior, paving the way to a standardized approach to assessing this critical rodent motor function in future studies.

Reaching into the future.

When carrying out a sequence of movements, humans can plan several steps in advance to make the movement smooth.

Impairments of social interaction in a valproic acid model in mice.

Background: A rodent autism spectrum disorder (ASD) model based on prenatal exposure to valproic acid (VPA) is widely recognized as a prominent model. Social behavior in rodent ASD models has primarily been evaluated through a three-chamber approach test. However, in this study, we focused on social attention in the VPA model of ASD. Methods: In male C57BL/6 J mice, attentional behaviors toward conspecifics were examined through reaching tasks around 9-11 weeks of age. On embryonic day 12.5, pregnant mice underwent a subcutaneous injection of 600 mg/kg VPA sodium salt dissolved in 0.9% saline solution (VPA group) or saline solution alone (Sal group) into their neck fat. Thirty-six mice-nine each in the VPA and saline groups, and 18 partners-underwent training in reaching behavior. Subsequently, we examined whether the VPA or Sal group demonstrated focused attention toward their partners during reaching tasks. A two-way analysis of variance (ANOVA) (condition [VPA/Sal] × situation [face-to-face (attention)/not paying attention (not attention)]) was conducted on the average success rate of the situation. Additionally, we measured the duration of sniffing behavior between pairs of mice in an open field twice in total at 4 and 8 weeks of age before reaching task. The pairs were constructed by pairing a VPA or Sal group mouse with its partner, with the objective of facilitating initial encounters between the mice. A one-way ANOVA was conducted on the average duration of sniffing behavior data from 4 weeks and a second one-way ANOVA on data from 8 weeks. Results: The analysis revealed a significant interaction between condition and situation in the reaching task [F (1, 28) = 6.75, p = 0.015, ηp 2 = 0.19]. The simple main effect test exhibited that the "not paying attention" rate was significantly higher than that of the "face-to-face" in the VPA group (p < 0.01). The results revealed a not significant difference in the average duration of sniffing behavior at 4 weeks [F (3, 32) = 2.71, p = 0.06, n.s., ηp 2 = 0.20], but significant difference at 8 weeks [F (3, 32) = 4.12, p < 0.05, ηp 2 = 0.28]. Multiple comparisons using the Bonferroni method revealed significant differences in the sniffing duration at 8 weeks between from the partner toward the VPA mouse and from the partner toward the Sal mouse (p < 0.05). Conclusion: The VPA rodent model of ASD exhibited differences in social attention compared to the saline group. By focusing on social attention and exploring various ASD models, insights can be gained from the neural mechanisms underlying gaze abnormalities during social interaction in individuals with ASD.

Future movement plans interact in sequential arm movements.

Real-world actions often comprise a series of movements that cannot be entirely planned before initiation. When these actions are executed rapidly, the planning of multiple future movements needs to occur simultaneously with the ongoing action. How the brain solves this task remains unknown. Here, we address this question with a new sequential arm reaching paradigm that manipulates how many future reaches are available for planning while controlling execution of the ongoing reach. We show that participants plan at least two future reaches simultaneously with an ongoing reach. Further, the planning processes of the two future reaches are not independent of one another. Evidence that the planning processes interact is twofold. First, correcting for a visual perturbation of the ongoing reach target is slower when more future reaches are planned. Second, the curvature of the current reach is modified based on the next reach only when their planning processes temporally overlap. These interactions between future planning processes may enable smooth production of sequential actions by linking individual segments of a long sequence at the level of motor planning.

Virtual reality assessment of reaching accuracy in patients with recent cerebellar stroke.

Background: Dysmetria, the inability to accurately estimate distance in motor tasks, is a characteristic clinical feature of cerebellar injury. Even though subjective dysmetria can be quickly detected during the neurological examination with the finger-to-nose test, objective quantification of reaching accuracy for clinical assessment is still lacking. Emerging VR technology allows for the delivery of rich multisensory environmental stimuli with a high degree of control. Furthermore, recent improvements in the hand-tracking feature offer an opportunity to closely examine the speed, accuracy, and consistency of fine hand movements and proprioceptive function. This study aims to investigate the application of virtual reality (VR) with hand tracking in the rapid quantification of reaching accuracy at the bedside for patients with cerebellar stroke (CS). Methods and results: Thirty individuals (10 CS patients and 20 age-matched neurologically healthy controls) performed a simple task that allowed us to measure reaching accuracy using a VR headset (Oculus Quest 2). During this task, the participant was asked to reach for a target placed along a horizontal sixty-degree arc. Once the fingertip passed through the arc, the target immediately extinguished. 50% of the trials displayed a visible, real-time rendering of the hand as the participant reached for the target (visible hand condition), while the remaining 50% only showed the target being extinguished (invisible hand condition). The invisible hand condition isolates proprioception-guided movements by removing the visibility of the participant's hand. Reaching error was calculated as the difference in degrees between the location of the target, and where the fingertip contacted the arc. Both CS patients and age-matched controls displayed higher average reaching error and took longer to perform a reaching motion in the invisible hand condition than in the visible hand condition. Reaching error was higher in CS than in controls in the invisible hand condition but not in the visible hand condition. Average time taken to perform each trial was higher in CS than in controls in the invisible hand conditions but not in the visible hand condition. Conclusions: Reaching accuracy assessed by VR offers a non-invasive and rapid approach to quantifying fine motor functions in clinical settings. Furthermore, this technology enhances our understanding of proprioceptive function in patients with visuomotor disabilities by allowing the isolation of proprioception from vision. Future studies with larger cohorts and longitudinal designs will examine the quantitative changes in reaching accuracy after stroke and explore the long-term benefits of VR in functional recovery.

Motor cortex is responsible for motoric dynamics in striatum and the execution of both skilled and unskilled actions.

Striatum and its predominant input, motor cortex, are responsible for the selection and performance of purposive movement, but how their interaction guides these processes is not understood. To establish its neural and behavioral contributions, we bilaterally lesioned motor cortex and recorded striatal activity and reaching performance daily, capturing the lesion's direct ramifications within hours of the intervention. We observed reaching impairment and an absence of striatal motoric activity following lesion of motor cortex, but not parietal cortex control lesions. Although some aspects of performance began to recover after 8-10 days, striatal projection and interneuronal dynamics did not-eventually entering a non-motor encoding state that aligned with persisting kinematic control deficits. Lesioned mice also exhibited a profound inability to switch motor plans while locomoting, reminiscent of clinical freezing of gait (FOG). Our results demonstrate the necessity of motor cortex in generating trained and untrained actions as well as striatal motoric dynamics.

Superior performance by two new methods in identifying the online reaction time of reaching movements.

Reaching movements can be redirected during their progress to handle unexpected visual changes, such as a change in target location. It is important to know when these redirections start, i.e., the online reaction time (oRT), but this information is not readily evident since redirections are embedded within a time-varying baseline movement that differs from trial to trial. The one previous study that evaluated the performance of different oRT identification methods utilized simulated redirections with the exact same onset, rather than a range of onsets as would be typically encountered. We addressed this gap by utilizing batches of "hybrid" trials with temporal spread in their oRTs. Each hybrid trial combined a sampled baseline movement with an idealized corrective response. Two new methods had the most accurate identification of online reaction times: 1) a threshold-aligned grand mean regression, and 2) a template-based approach we term the canonical correction search. The threshold-aligned grand mean regression is simple to implement and effective. The canonical correction search is a more complex procedure but arguably better linked to the underlying response. Applying the two methods to a published dataset revealed more delayed oRTs than was previously reported along with new information such as the width of oRT distributions. Taken together, our results demonstrate the utility of two new methods for dissecting corrective action from ongoing movement.NEW & NOTEWORTHY Advancing our understanding of visual feedback control requires methods that accurately identify the onset of corrective action. We developed a modified regression approach and a template-based approach to identify the online reaction time of single-reaching movements. Both outperform previous methods when challenged by temporal jitter in the response onset and increased background noise.

Robotic assessment of bilateral and unilateral upper limb functions in adults with cerebral palsy.

BACKGROUND: Children with unilateral cerebral palsy (CP) exhibit motor impairments predominantly on one side of the body, while also having ipsilesional and bilateral impairments. These impairments are known to persist through adulthood, but their extent have not been described in adults with CP. This study's aim is to characterize bilateral and unilateral upper limbs impairments in adults with CP. METHODS: Nineteen adults with CP (34.3 years old ± 11.5) performed three robotic assessments in the Kinarm Exoskeleton Lab, including two bilateral tasks (Object Hit [asymmetric independent goals task] and Ball on Bar [symmetric common goal task]) and one unilateral task (Visually Guided Reaching, performed with the more affected arm [MA] and less affected arm [LA]). Individual results were compared to sex, age and handedness matched normative data, describing the proportion of participants exhibiting impairments in each task-specific variable (e.g., Hand speed), each performance category (e.g., Feedforward control) and in global task performance. Associations were assessed using Spearman correlation coefficients between: 1: the results of the MA and LA of each limb in the unilateral task; and 2: the results of each limb in the unilateral vs. the bilateral tasks. RESULTS: The majority of participants exhibited impairments in bilateral tasks (84%). The bilateral performance categories (i.e., Bimanual) identifying bilateral coordination impairments were impaired in the majority of participants (Object Hit: 57.8%; Ball on Bar: 31.6%). Most of the participants were impaired when performing a unilateral task with their MA arm (63%) and a smaller proportion with their LA arm (31%). The Feedforward control was the unilateral performance category showing the highest proportion of impaired participants while displaying the strongest relationship between the MA and LA arms impairments (rs = 0.93). Feedback control was the unilateral performance category most often associated with impairments in bilateral tasks (6 out of 8 performance categories). CONCLUSIONS: Adults with CP experienced more impairment in bilateral tasks while still having substantial impairments in unilateral tasks. They frequently display Feedforward control impairments combined with a higher reliance on Feedback control during both bilateral and unilateral tasks, leading to poorer motor performance.

Level of decision confidence shapes motor memory.

Decision making is often necessary before performing an action. Traditionally, it has been assumed that decision making and motor control are independent, sequential processes. Ogasa et al. challenge this view, and demonstrate that the decision-making process significantly impacts on the formation and retrieval of motor memory by tagging it with the level of confidence.

Psychometric properties of the modified reaching performance scale in persons with multiple sclerosis.

BACKGROUND: A valid and reliable assessment tool to describe the quality of the movement pattern of reaching can provide valuable insights into motor performance deficits in persons with MS (pwMS). The Reaching Performance Scale, developed for stroke, is a promising scale to assess movement patterns in pwMS. However, psychometric properties of the scale are lacking in pwMS. OBJECTIVES: Firstly, to investigate the content validity of the modified Reaching Performance Scale for application in patients with MS (mRPS). Secondly, to investigate the psychometric properties (within- and between-session reliability and concurrent validity) of the mRPS for pwMS. METHODS: Forty-five pwMS (mean EDSS 6.6 pt, IQR 6-7.5) executed the mRPS that rates the quality of movement patterns and compensations during reach to grasp tasks. The content validity was determined by an expert panel based on observations of subjects performing the RPS. The reliability was based on five repetitions within one day, and between two days. For the concurrent validity, outcome measures at two levels of the International Classification of Functioning were correlated with the mRPS: Body Structure and Function level: Fugl-Meyer Assessment of the Upper Limb (FMA-UL), maximal isometric hand grip strength (HGS; Activity level: Action Research Arm Test (ARAT), Box and Blocks Test (BBT), Nine Hole Peg Test (NHPT) and Trunk Impairment Scale 2.0 (TIS 2.0) as well as perceived performance by the Manual Ability Measure-36 (MAM-36). RESULTS: Scale modifications were made only on the ratings of the trunk displacement subscale. The mRPS had excellent agreement scores for within-session reliability (range of Kappa between 0.85 and 0.98) and moderate-to-excellent agreement scores for between-session reliability (K: 0.66-1.00). Regarding validity, the mRPS was highly correlated with the ARAT (rho=0.74, p < 0.001), followed by moderate correlations with trunk performance (TIS 2.0, rho= 0.61, p < 0.001), hand function (BBT: rho=0.64, p < 0.001; NHPT: rho=-0.61, p < 0.001) and perceived performance (MAM36 rho= 0.53, p < 0.001). CONCLUSION: The mRPS is a reliable measurement tool to describe the movement pattern quality and motor compensations used during reaching in pwMS. Concerning concurrent validity, the mRPS is partially related to other measures of upper limb and trunk performance.

Medication improves velocity, reaction time, and movement time but not amplitude or error during memory-guided reaching in Parkinson's disease.

The motor impairments experienced by people with Parkinson's disease (PD) are exacerbated during memory-guided movements. Despite this, the effect of antiparkinson medication on memory-guided movements has not been elucidated. We evaluated the effect of antiparkinson medication on motor control during a memory-guided reaching task with short and long retention delays in participants with PD and compared performance to age-matched healthy control (HC) participants. Thirty-two participants with PD completed the motor section of the Movement Disorder Society Unified Parkinson's Disease Rating Scale (MDS-UPDRS III) and performed a memory-guided reaching task with two retention delays (0.5 s and 5 s) while on and off medication. Thirteen HC participants completed the MDS-UPDRS III and performed the memory-guided reaching task. In the task, medication increased movement velocity, decreased movement time, and decreased reaction time toward what was seen in the HC. However, movement amplitude and reaching error were unaffected by medication. Shorter retention delays increased movement velocity and amplitude, decreased movement time, and decreased error, but increased reaction times in the participants with PD and HC. Together, these results imply that antiparkinson medication is more effective at altering the neurophysiological mechanisms controlling movement velocity and reaction time compared with other aspects of movement control.

Decline in Sensory Integration in Old Age and Its Related Functional Brain Connectivity Correlates Observed during a Virtual Reality Task.

Sensory integration is an essential human function whose decline impacts quality of life, particularly in older adults. Herein, we propose an arm-reaching task based on a virtual reality head-mounted display system to assess sensory integration in daily life, and we examined whether reaching task performance was associated with resting-state functional connectivity (rsFC) between the brain regions involved in sensory integration. We hypothesized that declining sensory integration would affect performance during a reaching task with multiple cognitive loads. Using a task in which a young/middle-aged group showed only small individual differences, older adults showed large individual differences in the gap angle between the reaching hand and the target position, which was used to assess sensory integration function. Additionally, rsfMRI data were used to identify correlations between rsFC and performance in older adults, showing that performance was correlated with connectivity between the primary motor area and the left inferior temporal gyrus and temporo-occipital region. Connectivity between areas is related to visuomotor integration; thus, the results suggest the involvement of visuomotor integration in the decline of sensory integration function and the validity of the gap angle during this VR reaching task as an index of functional decline.

Measures of Implicit and Explicit Adaptation Do Not Linearly Add.

Moving effectively is essential for any animal. Thus, many different kinds of brain processes likely contribute to learning and adapting movement. How these contributions are combined is unknown. Nevertheless, the field of motor adaptation has been working under the assumption that measures of explicit and implicit motor adaptation can simply be added in total adaptation. While this has been tested, we show that these tests were insufficient. We put this additivity assumption to the test in various ways and find that measures of implicit and explicit adaptation are not additive. This means that future studies should measure both implicit and explicit adaptation directly. It also challenges us to disentangle how various motor adaptation processes do combine when producing movements and may have implications for our understanding of other kinds of learning as well (data and code: https://osf.io/3yhw5).

Feature evaluation for myoelectric pattern recognition of multiple nearby reaching targets.

Intention detection of the reaching movement is considerable for myoelectric human and machine collaboration applications. A comprehensive set of handcrafted features was mined from windows of electromyogram (EMG) of the upper-limb muscles while reaching nine nearby targets like activities of daily living. The feature selection-based scoring method, neighborhood component analysis (NCA), selected the relevant feature subset. Finally, the target was recognized by the support vector machine (SVM) model. The classification performance was generalized by a nested cross-validation structure that selected the optimal feature subset in the inner loop. According to the low spatial resolution of the target location on display and following the slight discrimination of signals between targets, the best classification accuracy of 77.11 % was achieved for concatenating the features of two segments with a length of 2 and 0.25 s. Due to the lack of subtle variation in EMG, while reaching different targets, a wide range of features was applied to consider additional aspects of the knowledge contained in EMG signals. Furthermore, since NCA selected features that provided more discriminant power, it became achievable to employ various combinations of features and even concatenated features extracted from different movement parts to improve classification performance.

Looking with or without seeing in an individual with age-related macular degeneration impairing central vision.

Looking leads gaze to objects; seeing recognizes them. Visual crowding makes seeing difficult or impossible before looking brings objects to the fovea. Looking before seeing can be guided by saliency mechanisms in the primary visual cortex (V1). We have proposed that looking and seeing are mainly supported by peripheral and central vision, respectively. This proposal is tested in an observer with central vision loss due to macular degeneration, using a visual search task that can be accomplished solely through looking, but is actually impeded through seeing. The search target is an uniquely oriented, salient, bar among identically shaped bars. Each bar, including the target, is part of an " " X " shape. The target's " X is identical to, although rotated from, the other " X 's in the image, which normally causes confusion. However, this observer exhibits no such confusion, presumably because she cannot see the " X 's shape, but can look towards the target. This result demonstrates a critical dichotomy between central and peripheral vision.

Characterization of bilateral reaching development using augmented reality games.

Bilateral coordination is commonly impaired in neurodevelopmental conditions including cerebral palsy, developmental coordination disorder, and autism spectrum disorder. However, we lack objective clinical assessments that can quantify bilateral coordination in a clinically feasible manner and determine age-based norms to identify impairments. The objective of this study was to use augmented reality and computer vision to characterize bilateral reaching abilities in typically developing children. Typically developing children (n = 133) ages 6-17 years completed symmetric and asymmetric bilateral reaching tasks in an augmented reality game environment. We analyzed the number of target pairs they could reach in 50 s as well as the time lag between their hands reaching the targets. We found that performance on both tasks developed in parallel, with development slowing but not plateauing after age 12. Children performed better on the symmetric task than asymmetric, both in targets reached and with shorter hand lags. Variability between children in hand lag decreased with age. We also found gender differences with females outperforming males, which were most pronounced in the 10-11 year olds. Overall, this study demonstrates parallel development through childhood and adolescence of symmetric and asymmetric reaching abilities. Furthermore, it demonstrates the ability to quantify bilateral coordination using computer vision and augmented reality, which can be applied to assess clinical populations.