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, 8 (2), 025027

Neural Control of Cursor Trajectory and Click by a Human With Tetraplegia 1000 Days After Implant of an Intracortical Microelectrode Array

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Neural Control of Cursor Trajectory and Click by a Human With Tetraplegia 1000 Days After Implant of an Intracortical Microelectrode Array

J D Simeral et al. J Neural Eng.

Abstract

The ongoing pilot clinical trial of the BrainGate neural interface system aims in part to assess the feasibility of using neural activity obtained from a small-scale, chronically implanted, intracortical microelectrode array to provide control signals for a neural prosthesis system. Critical questions include how long implanted microelectrodes will record useful neural signals, how reliably those signals can be acquired and decoded, and how effectively they can be used to control various assistive technologies such as computers and robotic assistive devices, or to enable functional electrical stimulation of paralyzed muscles. Here we examined these questions by assessing neural cursor control and BrainGate system characteristics on five consecutive days 1000 days after implant of a 4 × 4 mm array of 100 microelectrodes in the motor cortex of a human with longstanding tetraplegia subsequent to a brainstem stroke. On each of five prospectively-selected days we performed time-amplitude sorting of neuronal spiking activity, trained a population-based Kalman velocity decoding filter combined with a linear discriminant click state classifier, and then assessed closed-loop point-and-click cursor control. The participant performed both an eight-target center-out task and a random target Fitts metric task which was adapted from a human-computer interaction ISO standard used to quantify performance of computer input devices. The neural interface system was further characterized by daily measurement of electrode impedances, unit waveforms and local field potentials. Across the five days, spiking signals were obtained from 41 of 96 electrodes and were successfully decoded to provide neural cursor point-and-click control with a mean task performance of 91.3% ± 0.1% (mean ± s.d.) correct target acquisition. Results across five consecutive days demonstrate that a neural interface system based on an intracortical microelectrode array can provide repeatable, accurate point-and-click control of a computer interface to an individual with tetraplegia 1000 days after implantation of this sensor.

Figures

Figure 1
Figure 1
Performance on the Radial-8 and mFitts1 tasks on five consecutive days in which the neural cursor was used for point and click target selection. Daily performance on the Radial-8 task was assessed as the proportion of correct target selections relative to the total number of targets selected (Selection Hit Rate, black) and as a proportion of the total number of targets presented (Total Hit Rate, blue, middle) in 10 min (9 min for Day 999). Daily performance on the mFitts1 task was similarly assessed as the proportion of successfully acquired targets relative to the total number of targets presented (Total Hit Rate, red, right) in 10 min.
Figure 2
Figure 2
The rate of target acquisition for two assessment tasks. (a) Item selection rate for the Radial-8 task (blue) and mFitts1 task (red) on each of 5 consecutive days (total correct selections divided by total task time). (b) The dependence of target selection time (measured from target appearance through click execution) on selection task difficulty for all 62 correct trials of the mFitts1 task for Day 1000. (c) Regression of selection time on task difficulty (as in (b)) for each day. The regression for Day 999 (dotted line) was non-significant. (d) The relationship between selection time and selection difficulty for all correct mFitts1 trials from the five days showing significant linear regression on the pooled data. (open circles indicate data from Day 999 for which the within-day regression was non-significant). (e) Target diameter and distance-to-target for all 22 mFitts1 error trials (circles) across the 5-day study. Short lines indicate minimum and maximum distances offered (correct and error trials) for each of the three target diameters.
Figure 3
Figure 3
Neural cursor kinematics for trials in the Radial-8 task on five consecutive days. (a) Trajectories for all correct center-to-peripheral and peripheral-to-center movements (thin lines) with mean trajectories (thick lines). Gray circles (targets) and black circle (neural cursor) are drawn to scale with the outlining box demarcating display screen limits. All correct trials (‘T’) are shown for each day and span 10 min except Day 999 which was terminated at 9 min. ‘U’ indicates the number of units in the decoding filter. (b) Histogram of Radial-8 cursor speeds computed from the decoded velocity estimate at every time step (bin = 6 pix s−1; 26 689 samples) in the Radial-8 task. Each colour shows the distribution from one of the five days.
Figure 4
Figure 4
Neural click performance. (a) Demonstration of cross-validation testing during filter building on Day 1000 showing the two appended 90 s click training blocks in which imagined cursor movement was interspersed with epochs of imagined grasp (red). At every time step the decoder computed a log likelihood ratio (blue) and generated a click whenever it crossed to exceed an algorithmically-determined threshold (black line). (b) Distribution of distances between the neural cursor and the edge of target for all clicks during the mFitts1 assessment task across all five days. The green bar indicates clicks on targets; red bars indicate non-productive clicks on the desktop. 71% of all clicks were on target; of the remaining non-productive clicks, 75% were within 40 pixels of the target (red bins = 20 pixels).
Figure 5
Figure 5
Recording array impedance measurements. (a) Histogram of impedance measurements for all 96 electrodes on five consecutive days. (b) Change in impedance (z-score) for each of 96 electrodes relative to early post-implant measurement. (c) Mean electrode impedances across five days (measured at 1 kHz). Layout corresponds to implanted 10 × 10 microelectrode array. Unlabeled black locations measured > 4 MΩ on all days and were nonfunctional. Corner electrode locations (black with label) were not connected in the 96-channel system.
Figure 6
Figure 6
Properties of recorded units. (a) Number of units sorted by the technician (black), used in the filter (dark gray, middle) and significantly directionally tuned during the Radial-8 task (light gray, right) for each day. (b) Histogram of mean firing rates for each of the 183 units that were sorted during the five days (within-day means across 9 min of training data). Bins are 2 s except left bin which is 1 s to contain those units with firing rates less than 1 Hz that were excluded from decoding filters. (c) Distribution of mean waveform amplitudes for all units during each day’s mFitts1 assessment task (all technician-sorted units, black; the subset of units used for decoding, gray). (d) The mean sorted waveform (blue) from each day’s mFitts1 task shown for electrodes on the array where units were sorted in at least one session during the 5-day study. The mean daily waveforms of each second unit sorted on an electrode are also overlaid (red). At each electrode location the number of days on which a unit was recorded (i.e. the number of mean waveforms depicted) is indicated for first units (first number) and second units (second number). Gray-filled locations denote electrodes with impedances above 4 MΩ on all five days which were considered nonfunctional. Corner positions (black) were not connected in this 96-channel system.
Figure 7
Figure 7
Changes in the spectral content of local field potentials associated with intended movement on Day 1000. (a) Trial-aligned mean spectrogram of the field potential recorded from one representative electrode during 10 min of the Radial-8 task. Time 0 indicates time of target presentation. Changes in power, relative to within-band power before target appearance, were computed in 1 Hz steps using overlapping windows. Colour indicates proportion of amplitude change for each frequency relative to pre-presentation baseline. Dark blue reveals suppression between 14~30 Hz evident 0.6~ 1.2after target appearncn Horizontal line marks the frequency exhibiting maximum suppression (15 Hz). (b) Single-trial field potential from the same electrode as in (a) aligned to target appearance (t= 0) and filtered (10–20 Hz, 8th order filter) to highlight changes in signal amplitude corresponding to the power suppression near 15 Hz. (c) Spectrograms as in (a) computed for each of 96 electrodes during the Radial-8 task (excluding frequencies below 2 Hz for clarity). Notations: (s) 30 electrodes with sorted units on this day, (x) seven putative failed electrodes with impedances ≫ 4 MΩ on all five days, (1) additional 8 electrodes with impedance > > 4 MΩ on this particular day, (2) 2 electrodes with impedance ~4 MΩ. Colour range identical to (a).
Figure 8
Figure 8
Directional tuning of spiking activity during neural cursor control. (a) A population raster depicting all spiking events (ticks) of 33 simultaneously-recorded units (rows) during neural cursor point-and-click to one target in the Radial-8 task on Day 1000. Target onset occurred at time 0 (left vertical line) and the trial ended with a click on target at 6.18 s (right vertical line). (b) Spiking activity for one unit during all center-out cursor movements in the Radial-8 task on Day 999 (data set 2008.08.25.15.13.42_96a). For each of 8 movement directions, each spiking event is depicted by a tick with one row of ticks for each movement. Trials are aligned at target onset (time 0, red vertical line). Histograms below tally spiking events across trials and are normalized by bin size (333 ms for this analysis) to yield firing rates. This unit has a preferred firing direction of 347° (based on spiking activity between 0.25 s and 3.75 s after target onset) as summarized by the von Mises tuning curve (center). (c) Directional tuning among all significantly-tuned units in the recorded population during the Radial-8 task on each of five consecutive days. For each tuned unit, preferred direction and tuning depth from the fitted von Mises model are depicted by arrow orientation and length, respectively (top row of figures; radius represents modulation depth of 1). The number of units with significant tuning in each of the eight cardinal task directions was summed in 45° bins (bottom row).

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