A simulation study on the effects of neuronal ensemble properties on decoding algorithms for intracortical brain-machine interfaces

Background: Intracortical brain-machine interfaces (BMIs) harness movement information by sensing neuronal activities using chronic microelectrode implants to restore lost functions to patients with paralysis. However, neuronal signals often vary over time, even within a day, forcing one to rebuild a BMI every time they operate it. The term "rebuild" means overall procedures for operating a BMI, such as decoder selection, decoder training, and decoder testing. It gives rise to a practical issue of what decoder should be built for a given neuronal ensemble. This study aims to address it by exploring how decoders' performance varies with the neuronal properties. To extensively explore a range of neuronal properties, we conduct a simulation study. Methods: Focusing on movement direction, we examine several basic neuronal properties, including the signal-to-noise ratio of neurons, the proportion of well-tuned neurons, the uniformity of their preferred directions (PDs), and the non-stationarity of PDs. We investigate the performance of three popular BMI decoders: Kalman filter, optimal linear estimator, and population vector algorithm. Results: Our simulation results showed that decoding performance of all the decoders was affected more by the proportion of well-tuned neurons that their uniformity. Conclusions: Our study suggests a simulated scenario of how to choose a decoder for intracortical BMIs in various neuronal conditions

A Review of Control Strategies in Closed-Loop Neuroprosthetic Systems

It has been widely recognized that closed-loop neuroprosthetic systems achieve more favourable outcomes for users then equivalent open-loop devices. Improved performance of tasks, better usability and greater embodiment have all been reported in systems utilizing some form of feedback. However the interdisciplinary work on neuroprosthetic systems can lead to miscommunication due to similarities in well established nomenclature in different fields. Here we present a review of control strategies in existing experimental, investigational and clinical neuroprosthetic systems in order to establish a baseline and promote a common understanding of different feedback modes and closed loop controllers. The first section provides a brief discussion of feedback control and control theory. The second section reviews the control strategies of recent Brain Machine Interfaces, neuromodulatory implants, neuroprosthetic systems and assistive neurorobotic devices. The final section examines the different approaches to feedback in current neuroprosthetic and neurorobotic systems

Unscented Kalman Filter for Brain-Machine Interfaces

Brain machine interfaces (BMIs) are devices that convert neural signals into commands to directly control artificial actuators, such as limb prostheses. Previous real-time methods applied to decoding behavioral commands from the activity of populations of neurons have generally relied upon linear models of neural tuning and were limited in the way they used the abundant statistical information contained in the movement profiles of motor tasks. Here, we propose an n-th order unscented Kalman filter which implements two key features: (1) use of a non-linear (quadratic) model of neural tuning which describes neural activity significantly better than commonly-used linear tuning models, and (2) augmentation of the movement state variables with a history of n-1 recent states, which improves prediction of the desired command even before incorporating neural activity information and allows the tuning model to capture relationships between neural activity and movement at multiple time offsets simultaneously. This new filter was tested in BMI experiments in which rhesus monkeys used their cortical activity, recorded through chronically implanted multielectrode arrays, to directly control computer cursors. The 10th order unscented Kalman filter outperformed the standard Kalman filter and the Wiener filter in both off-line reconstruction of movement trajectories and real-time, closed-loop BMI operation

Learning and adaptation in brain machine interfaces

Balancing subject learning and decoder adaptation is central to increasing brain machine interface (BMI) performance. We addressed these complementary aspects in two studies: (1) a learning study, in which mice modulated “beta” band activity to control a 1D auditory cursor, and (2) an adaptive decoding study, in which a simple recurrent artificial neural network (RNN) decoded intended saccade targets of monkeys. In the learning study, three mice successfully increased beta band power following trial initiations, and specifically increased beta burst durations from 157 ms to 182 ms, likely contributing to performance. Though the task did not explicitly require specific movements, all three mice appeared to modulate beta activity via active motor control and had consistent vibrissal motor cortex multiunit activity and local field potential relationships with contralateral whisker pad electromyograms. The increased burst durations may therefore by a direct result of increased motor activity. These findings suggest that only a subset of beta rhythm phenomenology can be volitionally modulated (e.g. the tonic “hold” beta), therefore limiting the possible set of successful beta neuromodulation strategies. In the adaptive decoding study, RNNs decoded delay period activity in oculomotor and working memory regions while monkeys performed a delayed saccade task. Adaptive decoding sessions began with brain-controlled trials using pre-trained RNN models, in contrast to static decoding sessions in which 300-500 initial eye-controlled training trials were performed. Closed loop RNN decoding performance was lower than predicted by offline simulations. More consistent delay period activity and saccade paths across trials were associated with higher decoding performance. Despite the advantage of consistency, one monkey’s delay period activity patterns changed over the first week of adaptive decoding, and the other monkey’s saccades were more erratic during adaptive decoding than during static decoding sessions. It is possible that the altered session paradigm eliminating eye-controlled training trials led to either frustration or exploratory learning, causing the neural and behavioral changes. Considering neural control and decoder adaptation of BMIs in these studies, future work should improve the “two-learner” subject-decoder system by better modeling the interaction between underlying brain states (and possibly their modulation) and the neural signatures representing desired outcomes

Neural Adaptation and the Effect of Interelectrode Spacing on Epidural Electrocorticography for Brain-Computer Interfaces

Electrocorticography: ECoG) is increasingly being identified as a safe and reliable recording technique for both Brain-Computer Interface: BCI) applications as well as neurophysiology studies. This thesis describes some of the first real-time closed-loop BCI studies of chronic ECoG in non-human primates. Epidural microECoG electrodes developed in our lab were implanted in three monkeys with the electrode array centered over primary motor cortex: M1). Monkeys were then trained to perform a one-dimensional BCI task. The BCI control scheme was independent of any prior screening for task-related activity. All three monkeys successfully learned to perform the task with multiple control configurations and each time gained significant performance in 10 days or less. Interelectrode distance between control electrodes was also tested for three different distances. 15 and 9 mm spacing resulted in equivalent performance while 3 mm saw a moderate but significant degradation in performance. Finally, post hoc analysis was performed to analyze various decoding parameters. While decoding parameters were generally well matched to the observed signals, several potential decoding improvements were identified. Overall, these results demonstrate the feasibility of epidural ECoG BCIs, highlight the importance of neural adaptation for BCI control, and quantify various metrics of a current ECoG BCI system to drive further studies

Synaptic Learning for Neuromorphic Vision - Processing Address Events with Spiking Neural Networks

Das Gehirn übertrifft herkömmliche Computerarchitekturen in Bezug auf Energieeffizienz, Robustheit und Anpassungsfähigkeit. Diese Aspekte sind auch für neue Technologien wichtig. Es lohnt sich daher, zu untersuchen, welche biologischen Prozesse das Gehirn zu Berechnungen befähigen und wie sie in Silizium umgesetzt werden können. Um sich davon inspirieren zu lassen, wie das Gehirn Berechnungen durchführt, ist ein Paradigmenwechsel im Vergleich zu herkömmlichen Computerarchitekturen erforderlich. Tatsächlich besteht das Gehirn aus Nervenzellen, Neuronen genannt, die über Synapsen miteinander verbunden sind und selbstorganisierte Netzwerke bilden. Neuronen und Synapsen sind komplexe dynamische Systeme, die durch biochemische und elektrische Reaktionen gesteuert werden. Infolgedessen können sie ihre Berechnungen nur auf lokale Informationen stützen. Zusätzlich kommunizieren Neuronen untereinander mit kurzen elektrischen Impulsen, den so genannten Spikes, die sich über Synapsen bewegen. Computational Neuroscientists versuchen, diese Berechnungen mit spikenden neuronalen Netzen zu modellieren. Wenn sie auf dedizierter neuromorpher Hardware implementiert werden, können spikende neuronale Netze wie das Gehirn schnelle, energieeffiziente Berechnungen durchführen. Bis vor kurzem waren die Vorteile dieser Technologie aufgrund des Mangels an funktionellen Methoden zur Programmierung von spikenden neuronalen Netzen begrenzt. Lernen ist ein Paradigma für die Programmierung von spikenden neuronalen Netzen, bei dem sich Neuronen selbst zu funktionalen Netzen organisieren. Wie im Gehirn basiert das Lernen in neuromorpher Hardware auf synaptischer Plastizität. Synaptische Plastizitätsregeln charakterisieren Gewichtsaktualisierungen im Hinblick auf Informationen, die lokal an der Synapse anliegen. Das Lernen geschieht also kontinuierlich und online, während sensorischer Input in das Netzwerk gestreamt wird. Herkömmliche tiefe neuronale Netze werden üblicherweise durch Gradientenabstieg trainiert. Die durch die biologische Lerndynamik auferlegten Einschränkungen verhindern jedoch die Verwendung der konventionellen Backpropagation zur Berechnung der Gradienten. Beispielsweise behindern kontinuierliche Aktualisierungen den synchronen Wechsel zwischen Vorwärts- und Rückwärtsphasen. Darüber hinaus verhindern Gedächtnisbeschränkungen, dass die Geschichte der neuronalen Aktivität im Neuron gespeichert wird, so dass Verfahren wie Backpropagation-Through-Time nicht möglich sind. Neuartige Lösungen für diese Probleme wurden von Computational Neuroscientists innerhalb des Zeitrahmens dieser Arbeit vorgeschlagen. In dieser Arbeit werden spikende neuronaler Netzwerke entwickelt, um Aufgaben der visuomotorischen Neurorobotik zu lösen. In der Tat entwickelten sich biologische neuronale Netze ursprünglich zur Steuerung des Körpers. Die Robotik stellt also den künstlichen Körper für das künstliche Gehirn zur Verfügung. Auf der einen Seite trägt diese Arbeit zu den gegenwärtigen Bemühungen um das Verständnis des Gehirns bei, indem sie schwierige Closed-Loop-Benchmarks liefert, ähnlich dem, was dem biologischen Gehirn widerfährt. Auf der anderen Seite werden neue Wege zur Lösung traditioneller Robotik Probleme vorgestellt, die auf vom Gehirn inspirierten Paradigmen basieren. Die Forschung wird in zwei Schritten durchgeführt. Zunächst werden vielversprechende synaptische Plastizitätsregeln identifiziert und mit ereignisbasierten Vision-Benchmarks aus der realen Welt verglichen. Zweitens werden neuartige Methoden zur Abbildung visueller Repräsentationen auf motorische Befehle vorgestellt. Neuromorphe visuelle Sensoren stellen einen wichtigen Schritt auf dem Weg zu hirninspirierten Paradigmen dar. Im Gegensatz zu herkömmlichen Kameras senden diese Sensoren Adressereignisse aus, die lokalen Änderungen der Lichtintensität entsprechen. Das ereignisbasierte Paradigma ermöglicht eine energieeffiziente und schnelle Bildverarbeitung, erfordert aber die Ableitung neuer asynchroner Algorithmen. Spikende neuronale Netze stellen eine Untergruppe von asynchronen Algorithmen dar, die vom Gehirn inspiriert und für neuromorphe Hardwaretechnologie geeignet sind. In enger Zusammenarbeit mit Computational Neuroscientists werden erfolgreiche Methoden zum Erlernen räumlich-zeitlicher Abstraktionen aus der Adressereignisdarstellung berichtet. Es wird gezeigt, dass Top-Down-Regeln der synaptischen Plastizität, die zur Optimierung einer objektiven Funktion abgeleitet wurden, die Bottom-Up-Regeln übertreffen, die allein auf Beobachtungen im Gehirn basieren. Mit dieser Einsicht wird eine neue synaptische Plastizitätsregel namens "Deep Continuous Local Learning" eingeführt, die derzeit den neuesten Stand der Technik bei ereignisbasierten Vision-Benchmarks erreicht. Diese Regel wurde während eines Aufenthalts an der Universität von Kalifornien, Irvine, gemeinsam abgeleitet, implementiert und evaluiert. Im zweiten Teil dieser Arbeit wird der visuomotorische Kreis geschlossen, indem die gelernten visuellen Repräsentationen auf motorische Befehle abgebildet werden. Drei Ansätze werden diskutiert, um ein visuomotorisches Mapping zu erhalten: manuelle Kopplung, Belohnungs-Kopplung und Minimierung des Vorhersagefehlers. Es wird gezeigt, wie diese Ansätze, welche als synaptische Plastizitätsregeln implementiert sind, verwendet werden können, um einfache Strategien und Bewegungen zu lernen. Diese Arbeit ebnet den Weg zur Integration von hirninspirierten Berechnungsparadigmen in das Gebiet der Robotik. Es wird sogar prognostiziert, dass Fortschritte in den neuromorphen Technologien und bei den Plastizitätsregeln die Entwicklung von Hochleistungs-Lernrobotern mit geringem Energieverbrauch ermöglicht

A Real-Time Brain-Machine Interface Combining Motor Target and Trajectory Intent Using an Optimal Feedback Control Design

Real-time brain-machine interfaces (BMI) have focused on either estimating the continuous movement trajectory or target intent. However, natural movement often incorporates both. Additionally, BMIs can be modeled as a feedback control system in which the subject modulates the neural activity to move the prosthetic device towards a desired target while receiving real-time sensory feedback of the state of the movement. We develop a novel real-time BMI using an optimal feedback control design that jointly estimates the movement target and trajectory of monkeys in two stages. First, the target is decoded from neural spiking activity before movement initiation. Second, the trajectory is decoded by combining the decoded target with the peri-movement spiking activity using an optimal feedback control design. This design exploits a recursive Bayesian decoder that uses an optimal feedback control model of the sensorimotor system to take into account the intended target location and the sensory feedback in its trajectory estimation from spiking activity. The real-time BMI processes the spiking activity directly using point process modeling. We implement the BMI in experiments consisting of an instructed-delay center-out task in which monkeys are presented with a target location on the screen during a delay period and then have to move a cursor to it without touching the incorrect targets. We show that the two-stage BMI performs more accurately than either stage alone. Correct target prediction can compensate for inaccurate trajectory estimation and vice versa. The optimal feedback control design also results in trajectories that are smoother and have lower estimation error. The two-stage decoder also performs better than linear regression approaches in offline cross-validation analyses. Our results demonstrate the advantage of a BMI design that jointly estimates the target and trajectory of movement and more closely mimics the sensorimotor control system.National Institutes of Health (U.S.) (NIH grant No.DP1-0D003646-01)National Institutes of Health (U.S.) (NIH grant R01-EB006385