Single-neuron-resolution population dynamics in human Broca’s area and motor cortex when preparing and producing speech

Speech is a highly sophisticated, uniquely human behavior. It represents one of our fastest and most coordinated motor behaviors and connects intimately to higher-order cognitive capabilities of translating one’s mental state into sequences meant to influence another’s. Our groups have recently made headway in understanding the computations through neural ensemble dynamics underlying speech by piggybacking this scientific endeavor on top of an ongoing clinical trial studying brain-computer interfaces (BCIs) as a means to restore lost communication in people with paralysis. Here we propose extending this strategy to study how population activity (>100 neurons) in the ventral precentral gyrus (vPCG, i.e., speech motor cortex) and the pars opercularis portion of the inferior frontal gyrus (IFG, which encompasses Broca’s area) prepares and produces speech. We further propose complementing this high-resolution, narrow-windows ensemble single-unit-resolution study in two chronically implanted BCI participants with short-term medium-resolution, wide-coverage local field potential recordings across the wider speech and language network of multiple participants who are undergoing stereoelectroencephalography (sEEG) recordings, and with high-resolution, scattered-coverage recordings via sEEG wire tips and potentially with Neuropixels recordings during deep brain stimulation placement procedures.

These multimodal, multi-area human recordings during speech will allow us to discover how speech sequences are represented in preparatory and movement-epoch activity in the vPCG and IFG, and to identify the neural population dynamics which transform speech preparation into speech production. Our analyses will span from first-ever characterizations of what individual neurons in these brain areas encode to neural ensemble analyses that apply the team’s strength in building both dynamical system models and recurrent neural network models of the neural data to reveal biologically plausible and interpretable descriptions of how the coordinated activity of many neurons implements the computations needed to produce speech. This parallels a line of investigation pursued by our group to understand how arm movements are prepared and controlled in macaques and in people.

Our interdisciplinary team is uniquely prepared to overcome the challenges inherent in measuring and modeling a complex human motor/cognitive process: We are two neurosurgeons (Henderson, Brandman), two systems neuroscientists (Stavisky, Shenoy) and two computational neuroscientists (Sussillo, Druckmann) working across two BCI clinical trial sites (Stanford and University of California, Davis) which are geographically close enough to facilitate close collaboration while still far enough apart to effectively double our participant recruitment catchment area. The Pilot Award will help us establish a bridge between the computations-through-dynamics investigations being pursued by the Jazayeri team primarily in animal models and our new studies of highly complex motor tasks in humans. This will pave the way for larger follow-up efforts to understand both the shared and unique aspects of human cognition. Lastly, while this proposal focuses on fundamental human neuroscience opportunities, we are also motivated by the translational impact that a better understanding of the neural basis of speaking will have in informing our strategy for building BCIs to restore patients’ lost speech.