Microscale recording from human motor cortex: implications for minimally invasive electrocorticographic brain-computer interfaces

Abstract

Object: There is a growing interest in the use of recording from the surface of the brain, known as electrocorticography (ECoG), as a practical signal platform for brain-computer interface application. The signal has a combination of high signal quality and long-term stability that may be the ideal intermediate modality for future application. The research paradigm for studying ECoG signals uses patients requiring invasive monitoring for seizure localization. The implanted arrays span cortex areas on the order of centimeters. Currently, it is unknown what level of motor information can be discerned from small regions of human cortex with microscale ECoG recording.

Methods: In this study, a patient requiring invasive monitoring for seizure localization underwent concurrent implantation with a 16-microwire array (1-mm electrode spacing) placed over primary motor cortex. Microscale activity was recorded while the patient performed simple contra- and ipsilateral wrist movements that were monitored in parallel with electromyography. Using various statistical methods, linear and nonlinear relationships between these microcortical changes and recorded electromyography activity were defined.

Results: Small regions of primary motor cortex (< 5 mm) carry sufficient information to separate multiple aspects of motor movements (that is, wrist flexion/extension and ipsilateral/contralateral movements).

Conclusions: These findings support the conclusion that small regions of cortex investigated by ECoG recording may provide sufficient information about motor intentions to support brain-computer interface operations in the future. Given the small scale of the cortical region required, the requisite implanted array would be minimally invasive in terms of surgical placement of the electrode array.

Fig. 1

Experimental setup showing the microelectrode dimensions, anatomical location based on reconstructed MR and CT images of implanted electrodes, and EMG recording electrodes on the arm.

Fig. 2

Separating contralateral and ipsilateral movements. The figure demonstrates the averaged time frequency amplitude difference that was statistically different between ipsi- and contralateral movements. The time frequency plots are shown for each microelectrode (numbered on the left and shown on the right). The most prominent differences were more often found in lower-frequency bands (< 40 Hz) and in Electrodes 1, 2, 8, 9, and 10.

Fig. 3

Separating wrist flexion and extension from the contralateral limb. The figure demonstrates the averaged mutual information between the frequency spectra of each individual microelectrode and the EMG recording from the dorsal and ventral aspect of the forearm. Dorsal EMG is associated with wrist extension and ventral EMG changes are associated with wrist flexion. Left: The time scale shows the shared mutual information over a range of 332 msec (ms) before and after the onset of movement. For contralateral wrist movements, there is an increased contribution from 20–30-Hz signal change prior to the onset of movement, which occurs diffusely in the majority of electrodes with wrist flexion that is not present with wrist extension. Additionally, Electrodes 1, 2, and 7–10 show a very low–frequency predominance associated with flexion that is not present with extension. Wrist extension on the other hand shows a notable broadband frequency information content from 10 to 50 Hz in Electrode 16 not present with flexion. These findings indicate that there are qualitative differences in cortical activity associated with flexion and extension in the contralateral (left) arm. Right: The time scale shows the shared mutual information over a range of 332 msec before and after the onset of movement. Ipsilateral wrist flexion and extension movements are more similar than that seen with contralateral wrist movements. There is an anatomically diffuse frequency component that largely precedes the onset of movement in a frequency range of 30–50 Hz. There is, however, a notable difference in Electrode 7 demonstrating higher-frequency information content associated with wrist extension not seen in flexion. These findings indicate that there are qualitative differences in cortical activity associated with flexion and extension in the ipsilateral (right) arm.

Fig. 4

Distinguishing spectral and anatomical patterns of flexion and extension across both arms. The figure shows the patterns of mutual information in terms of anatomical location and frequency on the microarray. The spectral information was separated into 4 separate frequency bands: low (1–12 Hz), intermediate (13–43 Hz), high (48–152 Hz), and very high (174–566 Hz). Each condition has a distinct anatomical pattern of cortical activity in terms of which electrode participates in encoding either ipsi- or contralateral wrist flexion or extension. Additionally, there is a different spectral representation between each of the 4 conditions. Contralateral movements seem to be more predominantly represented by the low-frequency band (1–12 Hz), whereas ipsilateral movements are more highly represented by the intermediate frequency band (13–43 Hz). Each had focal high-frequency changes that were anatomically distinct to the given condition.