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

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.