Journal Article

Neural ensemble dynamics in dorsal motor cortex during speech in people with paralysis

Stavisky, Sergey D, Druckmann, Shaul, Shenoy, Krishna V, Henderson, Jaimie M, Avansino, Donald T, Memberg, William D, Wilson, Guy H, Ajiboye, A Bolu, Murphy, Brian A, Kirsch, Robert F, Willett, Francis R, Rezaii, Paymon, Miller, Jonathan P, Hochberg, Leigh R

2019

Overview

Speaking is a sensorimotor behavior whose neural basis is difficult to study with single neuron resolution due to the scarcity of human intracortical measurements. We used electrode arrays to record from the motor cortex ‘hand knob’ in two people with tetraplegia, an area not previously implicated in speech. Neurons modulated during speaking and during non-speaking movements of the tongue, lips, and jaw. This challenges whether the conventional model of a ‘motor homunculus’ division by major body regions extends to the single-neuron scale. Spoken words and syllables could be decoded from single trials, demonstrating the potential of intracortical recordings for brain-computer interfaces to restore speech. Two neural population dynamics features previously reported for arm movements were also present during speaking: a component that was mostly invariant across initiating different words, followed by rotatory dynamics during speaking. This suggests that common neural dynamical motifs may underlie movement of arm and speech articulators. Speaking involves some of the most precise and coordinated movements humans make. Learning how the brain produces speech could lead to better treatments for speech disorders. But it can be challenging to study. Human speech is unique, limiting what can be learned from animal studies. There also are few opportunities where it would be safe or ethical to take measurements from inside a person’s brain while they talk. Most previous studies have recorded brain activity during speech in patients who have had electrodes placed in the brain for epilepsy or Parkinson’s disease treatment. Now, Stavisky et al. show that brain cells that control hand and arm movements are also active during speech. Two patients who had lost the use of their arms and legs but were able to speak participated in the study. The two individuals were already enrolled in a pilot clinical trial of a brain-computer interface to help them control prosthetic devices. As part of this trial, the volunteer participants had two 100-electrode arrays surgically placed in the part of the brain that controls the movement of the arms and hands. This study made the unexpected discovery that brain cells multitask controlling not just arm and hand movements, but also carry information about movements of the lips, tongue and mouth necessary for speech. Stavisky et al. also found similarities in the patterns of brain activity during hand and arm movements and speech. By analyzing the activity in these brain cells as the two individuals recited words and syllables, Stavisky et al. were also able to train computers to identify which sound the person spoke from the brain activity alone. This is a first step towards developing a technology that could synthesize speech from a person’s brain activity as they try to speak. Much more work is needed to synthesize continuous speech. But the study provides initial evidence that it might be possible to use recordings from inside the brain to one day restore speech to individuals who have lost it.

• Publisher: eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Algorithms / Arm / Arm - physiopathology / Behavior / brain-computer interface / Brain-Computer Interfaces / Cortex (motor) / Electrocorticography / Electrodes / Hand - physiopathology / Homunculus / Human Biology and Medicine / Humans / Interfaces / intracortical / Jaw / Lip - physiopathology / Models, Neurological / motor control / motor cortex / Motor Cortex - physiopathology / Movement - physiology / Nerve Net - physiopathology / neural dynamics / Neurons / Neuroscience / Paralysis / Population / Population dynamics / Quadriplegia - physiopathology / Sensorimotor Cortex - physiopathology / Sensorimotor system / Speaking / Speech / Speech - physiology / Tongue - physiopathology