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Motor cortical beta oscillations have been reported for decades, yet their behavioral correlates remain unresolved. Some studies link beta oscillations to changes in underlying neural activity, but the specific behavioral manifestations of these reported changes remain elusive. To investigate how changes in population neural activity, beta oscillations, and behavior are linked, we recorded multi-scale neural activity from motor cortex while three macaques performed a novel neurofeedback task. Subjects volitionally brought their beta oscillatory power to an instructed state and subsequently executed an arm reach. Reaches preceded by a reduction in beta power exhibited significantly faster movement onset times than reaches preceded by an increase in beta power. Further, population neural activity was found to shift farther from a movement onset state during beta oscillations that were neurofeedback-induced or naturally occurring during reaching tasks. This finding establishes a population neural basis for slowed movement onset following periods of beta oscillatory activity.

During motor learning, movements and underlying neural activity initially exhibit large trial-to-trial variability that decreases over learning. However, it is unclear how task-relevant neural populations coordinate to explore and consolidate activity patterns. Exploration and consolidation could happen for each neuron independently, across the population jointly, or both. We disambiguated among these possibilities by investigating how subjects learned de novo to control a brain-machine interface using neurons from motor cortex. We decomposed population activity into the sum of private and shared signals, which produce uncorrelated and correlated neural variance, respectively, and examined how these signals' evolution causally shapes behavior. We found that initially large trial-to-trial movement and private neural variability reduce over learning. Concomitantly, task-relevant shared variance increases, consolidating a manifold containing consistent neural trajectories that generate refined control. These results suggest that motor cortex acquires skillful control by leveraging both independent and coordinated variance to explore and consolidate neural patterns., (Copyright © 2017 Elsevier Inc. All rights reserved.)

Objective: Movements made by healthy individuals can be characterized as superpositions of smooth bell-shaped velocity curves. Decomposing complex movements into these simpler "submovement" building blocks is useful for studying the neural control of movement as well as measuring motor impairment due to neurological injury., Approach: One prevalent strategy to submovement decomposition is to formulate it as an optimization problem. This optimization problem is nonconvex and finding an exact solution is computationally burdensome. We build on previous literature that generated approximate solutions to the submovement optimization problem., Results: First, we demonstrate broad conditions on the submovement building block functions that enable the optimization variables to be partitioned into disjoint subsets, allowing for a faster alternating minimization solution. Specifically, the amplitude parameters of a submovement can typically be fit independently of its shape parameters. Second, we develop a method to concentrate the search in regions of high error to make more efficient use of optimization routine iterations., Conclusion: Both innovations result in substantial reductions in computation time across multiple nonhuman primate subjects and diverse task conditions., Significance: These innovations may accelerate analysis of submovements for basic neuroscience and enable real-time applications of submovement decomposition.

Brain-machine interfaces (BMIs) aim to help people with paralysis by decoding movement-related neural signals into control signals for guiding computer cursors, prosthetic arms, and other assistive devices. Despite compelling laboratory experiments and ongoing FDA pilot clinical trials, system performance, robustness, and generalization remain challenges. We provide a perspective on how two complementary lines of investigation, that have focused on decoder design and neural adaptation largely separately, could be brought together to advance BMIs. This BMI paradigm should also yield new scientific insights into the function and dysfunction of the nervous system., (Copyright © 2014 Elsevier Inc. All rights reserved.)

Muscle synergies have been proposed as a mechanism to simplify movement control. Whether these coactivation patterns have any physiological reality within the nervous system remains unknown. Here we applied electrical microstimulation to motor cortical areas of rhesus macaques to evoke hand movements. Movements tended to converge toward particular postures, driven by synchronous bursts of muscle activity. Across stimulation sites, the muscle activations were reducible to linear sums of a few basic patterns-each corresponding to a muscle synergy evident in voluntary reach, grasp, and transport movements made by the animal. These synergies were represented nonuniformly over the cortical surface. We argue that the brain exploits these properties of synergies-postural equivalence, low dimensionality, and topographical representation-to simplify motor planning, even for complex hand movements., (Copyright © 2012 Elsevier Inc. All rights reserved.)

Closed-loop decoder adaptation (CLDA) shows great promise to improve closed-loop brain-machine interface (BMI) performance. Developing adaptation algorithms capable of rapidly improving performance, independent of initial performance, may be crucial for clinical applications where patients have limited movement and sensory abilities due to motor deficits. Given the subject-decoder interactions inherent in closed-loop BMIs, the decoder adaptation time-scale may be of particular importance when initial performance is limited. Here, we present SmoothBatch, a CLDA algorithm which updates decoder parameters on a 1-2 min time-scale using an exponentially weighted sliding average. The algorithm was experimentally tested with one nonhuman primate performing a center-out reaching BMI task. SmoothBatch was seeded four ways with varying offline decoding power: 1) visual observation of a cursor ( n = 20), 2) ipsilateral arm movements ( n = 8), 3) baseline neural activity ( n = 17), and 4) arbitrary weights ( n = 11). SmoothBatch rapidly improved performance regardless of seeding, with performance improvements from 0.018 ±0.133 successes/min to > 8 successes/min within 13.1 ±5.5 min ( n = 56). After decoder adaptation ceased, the subject maintained high performance. Moreover, performance improvements were paralleled by SmoothBatch convergence, suggesting that CLDA involves a co-adaptation process between the subject and the decoder.

Redundant encoding of information facilitates reliable distributed information processing. To explore this hypothesis in the motor system, we applied concepts from information theory to quantify the redundancy of movement-related information encoded in the macaque primary motor cortex (M1) during natural and neuroprosthetic control. Two macaque monkeys were trained to perform a delay center-out reaching task controlling a computer cursor under natural arm movement (manual control, 'MC'), and using a brain-machine interface (BMI) via volitional control of neural ensemble activity (brain control, 'BC'). During MC, we found neurons in contralateral M1 to contain higher and more redundant information about target direction than ipsilateral M1 neurons, consistent with the laterality of movement control. During BC, we found that the M1 neurons directly incorporated into the BMI ('direct' neurons) contained the highest and most redundant target information compared to neurons that were not incorporated into the BMI ('indirect' neurons). This effect was even more significant when comparing to M1 neurons of the opposite hemisphere. Interestingly, when we retrained the BMI to use ipsilateral M1 activity, we found that these neurons were more redundant and contained higher information than contralateral M1 neurons, even though ensembles from this hemisphere were previously less redundant during natural arm movement. These results indicate that ensembles most associated to movement contain highest redundancy and information encoding, which suggests a role for redundancy in proficient natural and prosthetic motor control.

Since its origins, the primary goal of transforming thought into action and sensation into perception has been to improve the quality of life for the physically impaired. Brain-machine interfaces (BMI) aim to improve the quality of life for large numbers of neurological patients. In particular, this novel technology is meant to play a major role in the near future as a serious contribution to spinal cord rehabilitation. During the last decade we have witnessed a dramatic increase in BMI research with impressive demonstrations of rodents, nonhuman primates, and humans controlling robots, wheelchairs, and graphical cursors in real time through signals collected from the brain. In this chapter we first review the different techniques used in the field of BMI, including electroencephalography (EEG), electrocorticography (ECoG), magnetoencephalography (MEG), and chronic multielectrode recordings. In addition we review the use of transcranial magnetic stimulation (TMS) for noninvasive modulation of excitability in relatively focal cortical areas. The chapter concludes with a discussion on the future implications of BMIs for directing functional movement and improving function after spinal injury in humans., (Copyright © 2012 Elsevier B.V. All rights reserved.)

Brain-machine interfaces (BMIs) provide a framework for studying cortical dynamics and the neural correlates of learning. Neuroprosthetic control has been associated with tuning changes in specific neurons directly projecting to the BMI (hereafter referred to as direct neurons). However, little is known about the larger network dynamics. By monitoring ensembles of neurons that were either causally linked to BMI control or indirectly involved, we found that proficient neuroprosthetic control is associated with large-scale modifications to the cortical network in macaque monkeys. Specifically, there were changes in the preferred direction of both direct and indirect neurons. Notably, with learning, there was a relative decrease in the net modulation of indirect neural activity in comparison with direct activity. These widespread differential changes in the direct and indirect population activity were markedly stable from one day to the next and readily coexisted with the long-standing cortical network for upper limb control. Thus, the process of learning BMI control is associated with differential modification of neural populations based on their specific relation to movement control.

Performing closed-loop modifications of a brain-machine interface (BMI) decoder is a technique that shows great promise for improving performance. We compare two algorithms for implementing adaptations that update decoder parameters on different time-scales (discrete batches vs. online), and present experimental results of a non-human primate performing a standard center-out BMI task. To ensure that our experimental training models are representative of a broad range of paralyzed patients, our decoders were initially trained using neural activity recorded during subject observation of cursor movement. We find that both closed-loop adaptation algorithms can be used to boost BMI performance from 20-30% to 80%, yielding movement kinematics similar to natural arm movements. Based on insights derived from the performance of each algorithm, we propose that a hybrid of batch and online decoder adaptation may be the best approach.

Research into the development of brain-machine interfaces (BMIs) has led to demonstrations of rodents, nonhuman primates, and humans controlling prosthetic devices in real time through modulation of neural signals. In particular, cortical BMI studies have shown that improvements in performance require learning and are associated with changes in neuronal tuning properties. These studies have further shown evidence of long-term improvements in performance with practice. The authors conducted experiments to understand long-term skill acquisition with BMIs and to characterize the neural correlates of improvements in task performance. They specifically assessed long-term acquisition of neuroprosthetic skill (i.e., accurate task performance readily recalled across days). In 2 monkeys performing a center-out task using a brain-controlled (BC) computer cursor, they closely monitored daily performance trends and the neural correlates under different conditions. Importantly, they assessed BC performance using a continuous-control multistep task. The authors first conducted experiments that mimicked experimental conditions commonly used. Specifically, a large set of neurons was incorporated with daily recalibration of the transform of neural activity to BC. Under such conditions, they found evidence of variable daily performance. In contrast, when a fixed transform was applied to stable recordings from an ensemble of neurons across days, there was consistent evidence of long-term skill acquisition. Such skill acquisition was associated with the crystallization of a cortical map for prosthetic control. Taken together, the results suggest that the primate motor cortex can achieve skilled control of a neuroprosthetic device through consolidation of a cortical representation.

A fundamental organizational principle of the primate motor system is cortical control of contralateral limb movements. Motor areas also appear to play a role in the control of ipsilateral limb movements. Several studies in monkeys have shown that individual neurons in primary motor cortex (M1) may represent, on average, the direction of movements of the ipsilateral arm. Given the increasing body of evidence demonstrating that neural ensembles can reliably represent information with a high temporal resolution, here we characterize the distributed neural representation of ipsilateral upper limb kinematics in both monkey and man. In two macaque monkeys trained to perform center-out reaching movements, we found that the ensemble spiking activity in M1 could continuously represent ipsilateral limb position. Interestingly, this representation was more correlated with joint angles than hand position. Using bilateral electromyography recordings, we excluded the possibility that postural or mirror movements could exclusively account for these findings. In addition, linear methods could decode limb position from cortical field potentials in both monkeys. We also found that M1 spiking activity could control a biomimetic brain-machine interface reflecting ipsilateral kinematics. Finally, we recorded cortical field potentials from three human subjects and also consistently found evidence of a neural representation for ipsilateral movement parameters. Together, our results demonstrate the presence of a high-fidelity neural representation for ipsilateral movement and illustrates that it can be successfully incorporated into a brain-machine interface.

Wireless sensors were designed which are small and light enough to be worn by small animals such as rats. These sensors are used to record three axes acceleration data from animals during natural behavior in a cage. The behavior of the animal is further extracted from the recorded acceleration data using neural network based pattern recognition algorithms. Successful recognition of eating, grooming and standing are demonstrated using this approach. Finally another potential application of this research is demonstrated in behavioral neuroscience by showing correlations between action potentials recorded from the motor cortex of a rat and acceleration data.

Research on brain-machine interfaces (BMI's) is directed toward enabling paralyzed individuals to manipulate their environment through slave robots. Even for able-bodied individuals, using a robot to reach and grasp objects in unstructured environments can be a difficult telemanipulation task. Controlling the slave directly with neural signals instead of a hand-master adds further challenges, such as uncertainty about the intended trajectory coupled with a low update rate for the command signal. To address these challenges, a continuous shared control (CSC) paradigm is introduced for BMI where robot sensors produce reflex-like reactions to augment brain-controlled trajectories. To test the merits of this approach, CSC was implemented on a 3-degree-of-freedom robot with a gripper bearing three co-located range sensors. The robot was commanded to follow eighty-three reach-and-grasp trajectories estimated previously from the outputs of a population of neurons recorded from the brain of a monkey. Five different levels of sensor-based reflexes were tested. Weighting brain commands 70% and sensor commands 30% produced the best task performance, better than brain signals alone by more than seven-fold. Such a marked performance improvement in this test case suggests that some level of machine autonomy will be an important component of successful BMI systems in general.

Significant variability in firing properties of individual neurons was observed while two monkeys, chronically implanted with multielectrode arrays in frontal and parietal cortical areas, performed a continuous arm movement task. Although the degree of correlation between the firing of single neurons and movement parameters was nonstationary, stable predictions of arm movements could be obtained from the activity of neuronal ensembles. This result adds support to the idea that movement parameters are redundantly encoded in the motor cortex, such that brain networks can achieve the same behavioral goals through different patterns and relative contribution of individual neuron activity. This has important implications for neural prosthetics, suggesting that accurate operation of a brain-machine interface requires recording from large neuronal ensembles to minimize the effect of variability and ensuring stable performance over long periods of time.

Monkeys can learn to directly control the movements of an artificial actuator by using a brain-machine interface (BMI) driven by the activity of a sample of cortical neurons. Eventually, they can do so without moving their limbs. Neuronal adaptations underlying the transition from control of the limb to control of the actuator are poorly understood. Here, we show that rapid modifications in neuronal representation of velocity of the hand and actuator occur in multiple cortical areas during the operation of a BMI. Initially, monkeys controlled the actuator by moving a hand-held pole. During this period, the BMI was trained to predict the actuator velocity. As the monkeys started using their cortical activity to control the actuator, the activity of individual neurons and neuronal populations became less representative of the animal's hand movements while representing the movements of the actuator. As a result of this adaptation, the animals could eventually stop moving their hands yet continue to control the actuator. These results show that, during BMI control, cortical ensembles represent behaviorally significant motor parameters, even if these are not associated with movements of the animal's own limb.

In the design of brain-machine interface (BMI) algorithms, the activity of hundreds of chronically recorded neurons is used to reconstruct a variety of kinematic variables. A significant problem introduced with the use of neural ensemble inputs for model building is the explosion in the number of free parameters. Large models not only affect model generalization but also put a computational burden on computing an optimal solution especially when the goal is to implement the BMI in low-power, portable hardware. In this paper, three methods are presented to quantitatively rate the importance of neurons in neural to motor mapping, using single neuron correlation analysis, sensitivity analysis through a vector linear model, and a model-independent cellular directional tuning analysis for comparisons purpose. Although, the rankings are not identical, up to sixty percent of the top 10 ranking cells were in common. This set can then be used to determine a reduced-order model whose performance is similar to that of the ensemble. It is further shown that by pruning the initial ensemble neural input with the ranked importance of cells, a reduced sets of cells (between 40 and 80, depending upon the methods) can be found that exceed the BMI performance levels of the full ensemble.

Evidence suggests that the CNS uses motor primitives to simplify movement control, but whether it actually stores primitives instead of computing solutions on the fly to satisfy task demands is a controversial and still-unanswered possibility. Also in contention is whether these primitives take the form of time-invariant muscle coactivations ("spatial" synergies) or time-varying muscle commands ("spatiotemporal" synergies). Here, we examined forelimb muscle patterns and motor cortical spiking data in rhesus macaques (Macaca mulatta) handling objects of variable shape and size. From these data, we extracted both spatiotemporal and spatial synergies using non-negative decomposition. Each spatiotemporal synergy represents a sequence of muscular or neural activations that appeared to recur frequently during the animals' behavior. Key features of the spatiotemporal synergies (including their dimensionality, timing, and amplitude modulation) were independently observed in the muscular and neural data. In addition, both at the muscular and neural levels, these spatiotemporal synergies could be readily reconstructed as sequential activations of spatial synergies (a subset of those extracted independently from the task data), suggestive of a hierarchical relationship between the two levels of synergies. The possibility that motor cortexmayexecute even complex skill using spatiotemporal synergies has novel implications for the design of neuroprosthetic devices, which could gain computational efficiency by adopting the discrete and low-dimensional control that these primitives imply. [ABSTRACT FROM AUTHOR]

Electrical microstimulation studies provide some of the most direct evidence for the neural representation of muscle synergies. These synergies, i.e., coordinated activations of groups of muscles, have been proposed as building blocks for the construction of motor behaviors by the nervous system. Intraspinal or intracortical microstimulation (ICMS) has been shown to evoke muscle patterns that can be resolved into a small set of synergies similar to those seen in natural behavior. However, questions remain about the validity of microstimulation as a probe of neural function, particularly given the relatively long trains of supratheshold stimuli used in these studies. Here, we examined whether muscle synergies evoked during ICMS in two rhesus macaques were similarly encoded by nearby motor cortical units during a purely voluntary behavior involving object reach, grasp, and carry movements. At each microstimulation site we identified the synergy most strongly evoked among those extracted from muscle patterns evoked over all microstimulation sites. For each cortical unit recorded at the same microstimulation site, we then identified the synergy most strongly encoded among those extracted from muscle patterns recorded during the voluntary behavior. We found that the synergy most strongly evoked at an ICMS site matched the synergy most strongly encoded by proximal units more often than expected by chance. These results suggest a common neural substrate for microstimulation-evoked motor responses and for the generation of muscle patterns during natural behaviors. [ABSTRACT FROM AUTHOR]