Accurate decoding of reaching movements from field potentials in the absence of spikes

Abstract

The recent explosion of interest in brain-machine interfaces (BMIs) has spurred research into choosing the optimal input signal source for a desired application. The signals with highest bandwidth--single neuron action potentials or spikes--typically are difficult to record for more than a few years after implantation of intracortical electrodes. Fortunately, field potentials recorded within the cortex (local field potentials, LFPs), at its surface (electrocorticograms, ECoG) and at the dural surface (epidural, EFPs) have also been shown to contain significant information about movement. However, the relative performance of these signals has not yet been directly compared. Furthermore, while it is widely postulated, it has not yet been demonstrated that these field potential signals are more durable than spike recordings. The aim of this study was to address both of these questions. We assessed the offline decoding performance of EFPs, LFPs and spikes, recorded sequentially, in primary motor cortex (M1) in terms of their ability to decode the target of reaching movements, as well as the endpoint trajectory. We also examined the decoding performance of LFPs on electrodes that are not recording spikes, compared with the performance when they did record spikes. Spikes were still present on some of the other electrodes throughout this study. We showed that LFPs performed nearly as well as spikes in decoding velocity, and slightly worse in decoding position and in target classification. EFP performance was slightly inferior to that reported for ECoG in humans. We also provided evidence demonstrating that movement-related information in the LFP remains high regardless of the ability to record spikes concurrently on the same electrodes. This is the first study to provide evidence that LFPs retain information about movement in the absence of spikes on the same electrodes. These results suggest that LFPs may indeed remain informative after spike recordings are lost, thereby providing a robust, accurate signal source for BMIs.

Figure 1

Positions of electrode arrays. (A) Monkey M’s intracortical array and superimposed epidural arrays (which were implanted in the contralateral hemisphere) with approximate electrode positions noted as black dots. (B) Monkey C’s epidural array, which was more anterior than monkey M’s array, and approximate intracortical array location (square). Approximate locations of stimulation that caused hand and arm movement during surgery and during sedation in the laboratory are denoted by star and circles, respectively. CS, central sulcus; AS, arcuate sulcus. Scale bars represent 2 mm.

Figure 2

Frequency domain features of field potentials. (A) Mean power spectra of LFPs and EFPs over all electrodes in one file of data each, with examples of raw LFP (green) and EFP (blue) on single channels (right). LFPs had substantially higher power in high-gamma bands than did EFPs. Despite this absolute power difference, ERSPs of single electrodes of (B, left) LFP and (C, left) EFP demonstrate that both EFPs and LFPs retain substantial relative power changes in delta (0–4 Hz), mu/beta (7–20 Hz) and high-gamma (>70 Hz) from just prior to movement onset (purple dashed line) to movement offset (black dashed line).

Figure 3

Examples of (A) position and (B) velocity decoding along the anterior-posterior (Y) axis using spikes, LFPs, and EFPs. Decoding with spikes and LFPs provided close matches to the actual position and velocity (left panels). While EFPs (right panels) tended to decode the general direction of the movement correctly, they missed the peaks of the data.

Figure 4

Continuous decoding performance in monkeys M and C for X and Y directions of (A) position and (B) velocity. Performance of LFPs was very similar to that of spikes in velocity estimation, somewhat worse in position estimation, while EFPs performed substantially poorer than either LFPs or spikes. (C) Velocity decoding performance for spikes, LFPs, and EFPs over time.

Figure 5

LFP decoding performance on electrodes in the presence or absence of spikes for (A) monkey M and (B) monkey C. Each dot represents the mean performance over 10 folds of one file. Lines connect pairs of files using the same set of electrodes when spikes are present (Spike, left) and absent (No Spike, right). (C) Contribution of frequency bands to the decoder was very similar for files with Spike (dashed lines) and No Spike (solid lines) in both monkeys.

Figure 6

Feature contributions to velocity decoding (measured as fraction of total decoder weights) for both monkeys (C, solid lines, M, dashed lines). (A) and (B), Relative weight as a function of time lag using LFPs and EFPs, respectively. (C) and (D), Relative weights of frequency bands (plotted on a log scale at the midpoint of each band, with LMP and 0–4 Hz band plotted at 1 and 4 Hz, respectively, for clarity) using LFPs and EFPs, respectively. Error bars show standard deviations. Asterisks denote time bins or frequency bands which differed significantly from the median fraction over all bins/bands for both monkeys (Wilcoxon signed-rank test, p<0.05).

Figure 7

Dependence of decoding performance on number of electrodes (for field potentials) or units (for spikes). The features (inputs) that correlated least with the output were dropped first from decoding. (A) In position decoding, LFPs and spikes both reached a plateau between 20 and 40 electrodes or units, respectively. Performance was somewhat different for X and Y position (thin and thick lines, respectively), especially for LFPs. For EFPs, decoding of both directions was similar and peaked by about 20 electrodes. These data are from one session with monkey M. (B) In velocity decoding, LFPs slightly outperformed spikes in this file. LFPs and EFPs reached maximum performance just before 20 electrodes.

Figure 8

Cross-correlation of frequency band power between electrode pairs for (A) LFPs and (B) EFPs. The LMP and lower frequency bands had the highest cross-correlation for both EFPs and LFPs, especially for LFPs. High-gamma bands had very low correlations for LFPs, and slightly higher for EFPs.

Figure 9

(A) Target decoding results for spikes, LFPs, and EFPs for both monkeys (C and M). Field potentials were decoded using all frequency bands. Dashed line represents chance performance determined empirically (14%). (B) Confusion matrices for EFPs, LFPs, and spikes averaged over all files in both monkeys. Color represents the fraction of decoded targets classified for each actual target. (C) Histogram of features used in target decoding with LFPs and EFPs. The high-gamma bands were used most with LFPs, while the 0–4 Hz band was used most in EFPs. Time bins at and shortly after movement onset were most highly weighted in both LFPs and EFPs.