Speech-related dorsal motor cortex activity does not interfere with iBCI cursor control

Abstract

Objective: Speech-related neural modulation was recently reported in 'arm/hand' area of human dorsal motor cortex that is used as a signal source for intracortical brain-computer interfaces (iBCIs). This raises the concern that speech-related modulation might deleteriously affect the decoding of arm movement intentions, for instance by affecting velocity command outputs. This study sought to clarify whether or not speaking would interfere with ongoing iBCI use.

Approach: A participant in the BrainGate2 iBCI clinical trial used an iBCI to control a computer cursor; spoke short words in a stand-alone speech task; and spoke short words during ongoing iBCI use. We examined neural activity in all three behaviors and compared iBCI performance with and without concurrent speech.

Main results: Dorsal motor cortex firing rates modulated strongly during stand-alone speech, but this activity was largely attenuated when speaking occurred during iBCI cursor control using attempted arm movements. 'Decoder-potent' projections of the attenuated speech-related neural activity were small, explaining why cursor task performance was similar between iBCI use with and without concurrent speaking.

Significance: These findings indicate that speaking does not directly interfere with iBCIs that decode attempted arm movements. This suggests that patients who are able to speak will be able to use motor cortical-driven computer interfaces or prostheses without needing to forgo speaking while using these devices.

Conflict of interest statement

Declaration of interests

K.V.S. consults for Neuralink Corp. and is on the scientific advisory boards of CTRL-Labs Inc., MIND-X Inc., Inscopix Inc., and Heal Inc. J.M.H. is a consultant for Neuralink Corp, Proteus Biomedical and Boston Scientific, and serves on the Medical Advisory Boards of Enspire DBS and Circuit Therapeutics. All other authors have no competing interests.

Figures

Figure 1.

Speech-related neural modulation in dorsal motor cortex is much weaker when occurring during ongoing BCI cursor control. (a) Task setup. We recorded speaking data and neural activity from a participant with two intracortical 96-electrode arrays implanted in the ‘hand knob’ area of motor cortex during BCI cursor control, during speaking, and during speaking while using the BCI. (b) Threshold crossing spike firing rates (mean ± s.e.) are shown for three example electrodes (rows) across three different behavioral contexts: 1) BCI cursor movement trials without any speaking (left column); 2) speaking alone (middle column); and 3) speaking at random times during ongoing BCI cursor control (right column). Cursor position traces from the corresponding trials are shown above the BCI column (one color per target). Trial-averaged acoustic spectrograms for one example word (“bat”) are shown above each speaking column. The acoustic spectrogram’s horizontal axis spans 100 ms before to 500 ms after acoustic onset, and its vertical axis spans 100 Hz to 10,000 Hz. Examples are from dataset T5.2018.12.17. (c) Summary of population firing rate changes (speaking minus silence, time-averaged over the 2 s epoch shown) when speaking alone (green) and when speaking during BCI use (blue). Each spoken word condition contributes one datum from each of the two datasets. Bars show the mean across all the dataset-conditions within each behavior.

Figure 2.

Speaking during ongoing BCI use has very little effect on cursor velocity decoder output. (a) Mean ‘neural push’ changes, i.e. the decoder-potent projection of firing rates that generated the cursor velocity, when making BCI cursor movements to each outward target (colors are the same as in figure 1b). Neural push traces shown in panels a, b, and c are from dataset T5.2018.12.17. (b) Neural push changes that would have occurred due to firing rate changes when speaking each of the five words, or silence (black), during stand-alone speech blocks, if the velocity decoder had been active. (c) Neural push changes aligned to speaking each of the five words, plus silence, when speaking occurred during the BCI cursor task. (d) Summary of neural push changes across the Radial 8 targets (orange) and word speaking conditions (green and blue) in both datasets. Silence conditions are shown separately as black markers (these lie very close to 0). Each dataset-condition contributes one datum based on its mean neural push change in the epoch shown with horizontal brackets in panels a - c. Bars show the mean across all the dataset-conditions within each behavior.

Figure 3.

Speaking during ongoing BCI use does not reduce cursor task performance. (a) Timeline of all BCI comparison blocks across two research sessions. Blue background denotes blocks in which the participant was instructed to speak after hearing an audio prompt; gray background denotes blocks with an instruction to not speak when hearing the prompt. Each dot shows one trial’s time to target. Trials during which a prompt was played are shown in red (if during a speaking block) or pink (if during a silent block). Horizontal bars show the median time to target of each block. Arrows on the right show the median across all trials of each instruction type. Orange ticks along the abscissa show when the decoder was recalibrated. (b) Box-and-whisker plots of times to target for ‘no cue’ trials that did not have an audio prompt, ‘prompted silent’ trials during a BCI silent block, and ‘prompted verbal’ trials during a BCI with speaking block. For each trial type, the center white line shows the distribution median, the thick (box) portion spans the 25th to 75th percentiles, and the thin lines (whiskers) extend another 1.5 times the box range. All remaining outlier points are shown as dots. Only the no prompt distribution was significantly different from that of the other two trial types (p < 0.001, rank-sum test). (c) Mean ± s.e. instantaneous absolute value cursor error angle aligned to the audio prompt that indicated when to speak (red), or not to speak (pink). As illustrated in the left side schematic, error angle is the angular difference between the instantaneous neural push and the vector pointing from the cursor to the target. 1 ms time bins in which there was a significant difference between the prompted silent and prompted verbal conditions are marked with a black tick above the traces (p < 0.01, rank-sum test). For comparison, no prompt trials are shown in gray (aligned to faux prompt times). Data are aggregated across both datasets. (d) Mean ± s.e. instantaneous cursor speeds for each trial type, aligned to the audio prompt, presented similarly to panel c.