NEUROSURGICAL FOCUS Neurosurg Focus 49 (1):E2, 2020 The current state of electrocorticography-based brain–computer interfaces Kai J. Miller, MD, PhD,1,2 Dora Hermes, PhD,2,3 and Nathan P. Staff, MD, PhD3 Departments of 1Neurosurgery, 2Physiology & Biomedical Engineering, and 3Neurology, Mayo Clinic, Rochester, Minnesota Brain–computer interfaces (BCIs) provide a way for the brain to interface directly with a computer. Many different brain signals can be used to control a device, varying in ease of recording, reliability, stability, temporal and spatial resolu- tion, and noise. Electrocorticography (ECoG) electrodes provide a highly reliable signal from the human brain surface, and these signals have been used to decode movements, vision, and speech. ECoG-based BCIs are being developed to provide increased options for treatment and assistive devices for patients who have functional limitations. Decoding ECoG signals in real time provides direct feedback to the patient and can be used to control a cursor on a computer or an exoskeleton. In this review, the authors describe the current state of ECoG-based BCIs that are approaching clinical viability for restoring lost communication and motor function in patients with amyotrophic lateral sclerosis or tetraplegia. These studies provide a proof of principle and the possibility that ECoG-based BCI technology may also be useful in the future for assisting in the cortical rehabilitation of patients who have suffered a stroke. https://thejns.org/doi/abs/10.3171/2020.4.FOCUS20185 KEYWORDS electrocorticography; brain–computer interface; BCI; amyotrophic lateral sclerosis; ALS; tetraplegia OR patients with functional limitations, the ability to ALS is a neurodegenerative disease in which the death use brain signals to control an assistive medical de- of motor neurons leads to progressive loss of muscle func- vice would greatly improve quality of life. Patients tion; advanced cases result in complete peripheral paraly- Fwith amyotrophic lateral sclerosis (ALS) or tetraplegia, sis (the locked-in syndrome [LIS]), which includes loss of for example, have significant impairments in communica- speech. Compared with movements of the body, extraocu- tion and motor control. For patients with ALS, eye track- lar movements are spared until later in the disease course ing may provide an option for these individuals to control for patients with ALS who have LIS, allowing for use of a device, but this technology depends on light conditions eye-tracking systems. The prevalence of ALS in the US and full ocular mobility, which may be limited in the late is 5 in 100,000 people;4 the median survival of patients stages of ALS.1 Two recent studies in electrocorticography with ALS is 2–3 years, with eventual death resulting from (ECoG)-based brain–computer interfaces (BCIs)—sys- respiratory failure. Studies have shown that patients with tems that record, amplify, and translate brain signals into LIS who can maintain self-initiated, open-ended commu- computer commands for external devices—offer hope to nication through electronic devices believe themselves to these patients for improved self-management of physical have a higher quality of life than those who are limited limitations by restoring communication or motor control to communicating by responding to questions from others capabilities.2,3 In this review, we primarily focus on 2 con- with a yes/no code.5 ditions with high functional impairment and morbidity— Tetraplegia (also called quadriplegia) is the paralysis of ALS and tetraplegia—for which BCI technology has been all 4 extremities and the torso as a result of injury to the implemented most extensively. cervical spinal cord. Every year an estimated 250,000– ABBREVIATIONS ALS = amyotrophic lateral sclerosis; BCI = brain–computer interface; ECoG = electrocorticography; EEG = electroencephalography; LIS = locked-in syndrome; WIMAGINE = Wireless Implantable Multichannel Acquisition system for Generic Interface with Neurons. SUBMITTED March 1, 2020. ACCEPTED April 20, 2020. INCLUDE WHEN CITING DOI: 10.3171/2020.4.FOCUS20185. ©AANS 2020, except where prohibited by US copyright law Neurosurg Focus Volume 49 • July 2020 1 Unauthenticated | Downloaded 10/06/21 09:37 AM UTC Miller et al. 500,000 individuals worldwide will have a spinal cord injury, most commonly caused by vehicular crashes, falls, or acts of violence.6 Nearly 50% of these individuals will have a spinal cord injury in the cervical region,7 and among individuals with a cervical spinal cord injury, 20% will be diagnosed with tetraplegia.2 In the US alone, there are more than 100,000 patients living with tetraplegia. The development of BCIs as a new communication and control mode for patients with severe loss of com- munication ability or motor function began 30 years ago with electroencephalography (EEG) electrodes placed on the scalp. These used either changes in the raw deflection of the voltage associated with attention to visual stimuli FIG. 1. Electrode types that have been used for BCIs: EEG from scalp, in navigating a decision matrix8 or movement-associated ECoG from brain surface, and cortex-penetrating microelectrodes. band-limited changes in the power spectrum of the volt- Copyright Kai J. Miller. Published with permission. age to control 1-dimensional cursor movement on a com- puter screen.9 EEG sensors (electrodes) for recording brain activity for BCIs are noninvasive and widely available, hospital for approximately 1 week while waiting for the they have a limited spatial resolution, and brain signals onset of another seizure. During this time they may volun- are relatively small compared to the noise, which reduces teer for studies that allow researchers to correlate strictly the single-trial decoding ability. At the opposite extreme defined tasks with resulting ECoG signals that (because are surgically placed microelectrodes that penetrate the the placement of the ECoG array is known) can be cor- cortex, measuring single neurons; these offer multidimen- 23,25 10–12 related with the structure of the brain. sional control of BCI devices. In their current form, ECoG-based BCIs may consist of the following com- these high-fidelity microelectrode signals require exter- ponents (Fig. 3):26 1) an implantable electrode array for nalized leads with connection to a research-grade experi- real-time recording and digitization of the brain signal; 2) mental rig. Due to issues of infection, biological rejection, a subcutaneous amplifier and transmitter unit (with leads and signal instability, these electrodes are still at the stage 13–15 connected to the electrode array) for wireless transmission of ongoing development. ECoG electrodes, placed of the digitized signal; 3) a Bluetooth-enabled, signal pro- subdurally on the arachnoidal surface of the brain, offer a cessing computer for real-time analysis of the signal and middle-ground signal between microelectrodes and EEG translation into computer commands; and 4) a computer- (Fig. 1). Modern ECoG research began with a 1998 study ized device that receives these commands and performs in which electrodes over the sensorimotor cortex detected an action that is now under the control of the patient (e.g., increases in high-frequency power during movement com- a tablet computer for communicating or Web browsing, an pared to rest.16,17 Currently, the use of subdural ECoG elec- exoskeleton, a robotic arm, or a wheelchair). Implantable trode arrays for BCIs provides a high signal-to-noise ratio ECoG electrode arrays for clinical use are commercially and a localized cortical signal (typically, clinical ECoG available from a number of sources—e.g., NeuroPace, arrays consist of electrodes 2.3 mm in diameter, placed 1 Medtronic, and PMT Corp.—as are some additional com- cm apart). ponents of the BCI system. Current trends of improved The identification of a strong, reproducible brain signal electrodes, as well as implants that are more standardized in an individual can be used as the basis for driving a BCI. and easier to place, are driving the ECoG-based BCI field ECoG measures the electrical potential on the surface of forward. the brain resulting from the sum of the local field poten- tials of the population of neurons directly underneath each Current Status of ECoG-Based BCI Studies electrode—approximately 500,000 for the most common clinical contact surface area of 5 mm.2,18 During active Current BCI devices are generally based on signals movement, the ECoG signal exhibits a superposition in- from 1 of 3 cortical areas: motor, vision, or speech. These cluding 2 characteristic changes that occur in the cortical demonstrations open possibilities for many other brain power spectrum and can be decoupled: 1) narrow-band functions and other general BCI applications such as cor- power decreases at frequencies < 40 Hz (alpha/mu and tical rehabilitation. beta rhythms) over large areas of the sensorimotor cor- tex;17,19,20 and 2) a broadband increase in power at frequen- Motor-Based Studies cies > 50 Hz over focal cortical areas16,19,21–23 (Fig. 2). The In studies with epileptic patients, imagined motor ECoG signal has demonstrated broadband increases in movement (imagery) has been shown to induce ECoG- power during activity, compared to rest, across a variety measured cortical activity change in primary motor areas of cortical regions and behavioral tasks.24 of the brain at a level approximately 25% of that induced Most of what has been learned about ECoG signals by the actual motor movement itself.27 Furthermore, when for driving BCIs has been from patients with medically these individuals learned to use imagery to control a cur- intractable epilepsy. These are individuals who undergo sor on a computer screen in a feedback-providing man- clinical ECoG for localization of the seizure focus prior ner, the cortical activity change induced by motor imagery to resection; after implantation they are monitored in the surpassed that from the actual movement. Several groups 2 Neurosurg Focus Volume 49 • July 2020 Unauthenticated | Downloaded 10/06/21 09:37 AM UTC Miller et al.