Brain-computer interfaces: military, neurosurgical, and ethical perspective

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Brain-computer interfaces (BCIs) are devices that acquire and transform neural signals into actions intended by the user. These devices have been a rapidly developing area of research over the past 2 decades, and the military has made significant contributions to these efforts. Presently, BCIs can provide humans with rudimentary control over computer systems and robotic devices. Continued advances in BCI technology are especially pertinent in the military setting, given the potential for therapeutic applications to restore function after combat injury, and for the evolving use of BCI devices in military operations and performance enhancement. Neurosurgeons will play a central role in the further development and implementation of BCIs, but they will also have to navigate important ethical questions in the translation of this highly promising technology. In the following commentary the authors discuss realistic expectations for BCI use in the military and underscore the intersection of the neurosurgeon's civic and clinical duty to care for those who serve their country.

Abbreviations used in this paper: BCI = brain-computer interface; DARPA = Defense Advanced Research Projects Agency; ECoG = electrocorticography; EEG = electroencephalography.

Brain-computer interfaces (BCIs) are devices that acquire and transform neural signals into actions intended by the user. These devices have been a rapidly developing area of research over the past 2 decades, and the military has made significant contributions to these efforts. Presently, BCIs can provide humans with rudimentary control over computer systems and robotic devices. Continued advances in BCI technology are especially pertinent in the military setting, given the potential for therapeutic applications to restore function after combat injury, and for the evolving use of BCI devices in military operations and performance enhancement. Neurosurgeons will play a central role in the further development and implementation of BCIs, but they will also have to navigate important ethical questions in the translation of this highly promising technology. In the following commentary the authors discuss realistic expectations for BCI use in the military and underscore the intersection of the neurosurgeon's civic and clinical duty to care for those who serve their country.

Abbreviations used in this paper: BCI = brain-computer interface; DARPA = Defense Advanced Research Projects Agency; ECoG = electrocorticography; EEG = electroencephalography.

Brain-computer interfaces, also called brain-machine interfaces or neural interface systems, represent a direct communication pathway between the brain and an external device.18,32,59 The devices used for the BCI acquire brain signals such as an EEG rhythm or electrophysiological recordings of neuronal firing and translate them into commands intended by the user. Brain-computer interfaces accomplish this through novel output pathways that do not use the normal conduits of the nervous system.32

During the past 40 years, BCIs have rapidly progressed from mere neuroscientific theory into a rudimentary yet highly promising technology. Increasing levels of brain-derived control have been attained in nonhuman primates and in humans.13,21,32,48,50,51,54,55 Moreover, rapid progress of supporting technologies from the fields of computational neuroscience, biomaterial engineering, and computer processing have significantly contributed to the ongoing development of BCIs. Importantly, an ever-increasing understanding of motor, cognitive, and sensory functions through cortical mapping has led to improvements in device designs as well as a wider gamut of possible BCI applications.32,42,43

Media hype and popular imagination regarding potential applications of BCIs have greatly exceeded the current state of the technology. Nevertheless, practical and clinically useful BCIs are increasingly becoming a reality, and this has important implications for neurosurgeons practicing and conducting research in military settings. Our aim in this commentary is to use an understanding of current achievements in the field of BCIs to discuss realistic expectations for future adaptation of BCI systems in military settings and to highlight the complex role of military neurosurgeons in the further expansion of this technology. The implications of neurosurgical BCI implantation for restoring function to injured soldiers as well as the potential to enhance military training and operations are considered from an ethical perspective. In the context of our national duty to support those who serve our country, we reinforce the importance of physician beneficence and nonmaleficence in any BCI application, alongside responsible and just distribution of the technology.

State of BCI Technology at Present

For BCIs to translate the user's intentions accurately into actions, “learning” must take place on both ends of the interface: the user must modulate his or her brain signals to improve performance of the BCI, while the device must identify, interpret, and adapt to the neural signals that are most predictive of the desired output. This is achieved through feedback and fine-tuning mechanisms that are similar to those used when learning a new motor task.32 Some BCI designs rely on a training phase in which the subject performs a designated task and a computational algorithm is employed to select the neuronal signals that best correlate with execution of that task. A code is generated for each command that can subsequently be used for control of an external device.31,39,40 Alternatively, a real-time adaptive algorithm can be employed during the learning phase to concurrently select for the signals that are most predictive of the user's intentions by continuously refining them based on comparisons of past and intended trajectories.40,54,60 Recordings from larger populations of neurons, or neuronal ensembles, are generally the preferred source for extracting useful and relevant information to guide appropriate activity.2,6,40 Although input from a single neuron can result in successful BCI control,7,22 averaging neuronal signals over many trial sessions is often necessary for predicting behavior,46 and therefore synthesizing the electrical firing of neuronal ensembles can remove the variability associated with using the input of a single neuron.2,40 As the user learns to operate the BCI, neuronal plasticity leads to a tuning of ensemble signals such that activity in more discrete populations of neurons becomes the best determinant of action commands.8,30

Depending on the source from which they derive their neural signals, BCIs can be classified into those that use noninvasive, invasive, and partially invasive platforms (Fig. 1). Electroencephalography, which obtains electrical signals from the scalp, has been the dominant method of recording used for noninvasive BCIs due to its relative safety and practical technical requirements. Invasive BCIs retrieve signals from single-neuron recordings via microelectrodes implanted in the cortical layers. Partially invasive BCIs use ECoG readings that come from sensors at the cortical surface placed either above or below the dura mater.10,32,40,48 Platforms that belong to the latter 2 classes require neurosurgical implantation.

Fig. 1.
Fig. 1.

Three classes of BCIs: their anatomical locations, advantages, and limitations.

Using an EEG-based system, humans with motor debilities, including those that result from spinal cord injury or amyotrophic lateral sclerosis, have been able to control a computer cursor in 2 dimensions.29,60 This technology has also been used by motor-intact individuals to command robots to manipulate objects, and has the potential to be applied in operating limb prosthetics.3 The EEG devices, however, are fundamentally limited by their signal content, which does not convey information about components of movement such as position and velocity, and recordings are prone to interference from the electromyographic activity of cranial musculature.10,32

Invasive BCIs, on the other hand, can acquire more informative signals that enable higher performance limits.50 For instance, human patients with locked-in syndrome are able to move cursors on a 2D keyboard to communicate using typed messages after undergoing implantation of electrodes that attract growth of myelinated nerve fibers.24,25 With the aid of a 96-microelectrode array that records signals from primary motor cortex, tetraplegic patients have been able to move a 2D cursor as well as to execute basic control over robotic devices, such as opening and closing a prosthetic hand, years after their initial spinal cord injury.21 Subsequent reports on tetraplegic patients who were enrolled in a pilot clinical trial of BCIs have demonstrated modest improvements in cursor control, thereby achieving greater functionality for practical tasks.13,26

More recently, ECoG has proven to be a useful tool in detecting input signals for BCIs.33,51 Unlike EEG, ECoG can detect high-frequency gamma wave activity that is the product of smaller cortical ensembles and correlates with discharge of action potentials from cortical neurons.19,32 Because they are not embedded in brain parenchyma, ECoG electrodes inflict less damage to the cortex and also experience less signal deterioration than invasive electrodes.32,34 In patients with intractable epilepsy who required invasive monitoring, ECoG signals have been used for 2D movement control at a level of performance similar to that achieved with invasive BCIs.51 Although this approach has not been tested in patients with motor impairment, it can be applied more safely than invasive electrodes, and produces greater information content than EEG systems.32

Although invasive and partially invasive BCIs hold great potential for functional recovery, the current risks and limitations associated with device implantation prevent BCIs from widespread use. One of the major shortcomings of the current technology is associated with the loss of signal reliability over time. In response to damage incurred by microelectrode penetration of the cortex, microglia and astrocytes begin a reactive process that ensheaths the prosthesis and disrupts its initial impedance properties.5,16,45,58 Neural and vascular damage at the site of insertion can also lead to development of infections.5,23 As a result, the length of time over which an implantable electrode is able to produce signals is measured in months, and typically does not make it over 1 year without significantly losing quality.48,53 Moreover, motion between the implanted electrode and brain parenchyma, as is often caused by changes in brain volume or physical activity, can influence signal production.49

The Future of BCI Therapeutics: Restoring Function After Combat Injury

Although BCI technology at present has had a narrow scope of application in a small group of severely impaired patients, robust research efforts are underway to overcome current limitations and to boost the effectiveness of invasive electrode platforms. For instance, the design of biocompatible microelectrode coatings27 and algorithms that can adapt to vigorous movement9 promises to endow BCIs with the durability needed to withstand commonplace disturbances encountered outside the confines of a controlled laboratory environment. Additionally, development of ECoG-based platforms constitutes an important investigative avenue, given their lower risk profile when compared with single-neuron electrodes and their higher information content than EEG studies.32 These properties would allow ECoG BCIs to be implanted in patients harboring less severe injury, and may make this the modality of choice in the future when restoring function to wounded soldiers.

The comparatively greater success of BCIs in animal studies further substantiates the potential for these devices to become functional prostheses. Rhesus monkeys implanted with electrodes recording from as few as 18 cortical neurons are able to move a cursor in 3 dimensions while also receiving visual feedback from their brain-controlled environment.54 In follow-up studies, implanted monkeys have also been trained to control a multijointed robotic arm to exert variable grip strength and perform 3D movements to feed themselves.55 These results have been achieved with motor prostheses, which continuously process cortical signals to guide movement and speed.48 Their counterparts, communication prostheses, which extract information from higher cortical areas about intended goals, have also been successful and promise to enhance BCI performance as it might be applied to humans executing more complicated goal-oriented tasks.17,37,48,50 The end point of the ongoing advances in BCIs lies in the translation of such functionality from preclinical studies to humans, and thus BCI research deserves continued academic and clinical attention as well as government funding to help those who risk their lives for their country.

Combat casualties from the wars in Afghanistan and Iraq have a marked propensity to present with the types of injuries that may be addressed with new developments in BCIs. Possibly in connection with increased use of body armor,15,28,44 the number of combat-related extremity injuries has been on the rise, representing 54% of all combat injuries and 63% of primary diagnoses for admission.41 In a recent analysis, Masini and colleagues35 concluded that extremity injuries are the leading cause of disability among soldiers not returning to duty, and have the greatest projected disability benefit costs. In addition, spinal cord injuries represent a significant proportion of casualties,56 occurring in nearly 10% of the entire caseload of closed or penetrating head trauma seen by military neurosurgeons in the US.4 Neuroprosthetic use of BCIs can directly address the major clinical problems affecting active soldiers, improve quality of life for those injured in combat, and ultimately reduce the individual, fiscal, and social impact of disability.

In the face of new developments in the field of BCIs, whether to take on the risks of surgery and implantation must remain a question of utmost clinical and ethical importance for a military neurosurgeon. Up to the present moment, BCI devices have been able to benefit only the most severely injured patients, such as those with locked-in syndrome or tetraplegia.21,24 It is only with improvements in the safety, longevity, and effectiveness of BCIs that neurosurgeons can begin to consider routine use of such devices, even for significantly disabled and willing soldiers. In any future discussion with a potential patient regarding BCI implantation, expectation management must be a central element of the conversation, because the clinical trial stage will still consider BCIs to be an experimental therapy rather than a treatment with confirmed benefits. Furthermore, in light of the increasing incidence of posttraumatic stress disorder and psychiatric issues experienced by veterans of recent wars,36 it will be crucial for military neurosurgeons to take into account the influence of mental health on decision making as well as any preconceived assumptions held by the patient about BCI treatments. Irrespective of the situation, any application of BCIs in humans must be conducted in accordance with the guiding principles of patient autonomy and informed consent as well as physician beneficence and nonmaleficence as espoused by the Hippocratic Oath, the Belmont Report, and the Declaration of Helsinki.14,38,61

Military Enhancement With BCIs

Alongside therapeutic interventions, rapid advances in BCI technologies will also create opportunities for neurosurgeons to participate in improving military training and operations, particularly through combat performance modification and optimization. In fact, the use of neuroscientific approaches for achieving these goals is already an evolving area of research. During the last decade, the Pentagon's DARPA launched the “Advanced Speech Encoding Program” to develop nonacoustic sensors for speech encoding in acoustically hostile environments, such as inside of a military vehicle or an urban environment.12 The DARPA division is currently involved in a program called “Silent Talk” that aims to develop user-to-user communication on the battlefield through EEG signals of “intended speech,” thereby eliminating the need for any vocalization or body gestures.11 Such capabilities will be of particular benefit in reconnaissance and special operations settings, and successful applications of silent speech interfaces have already been reported.12

Enhancements of soldiers' perception and control of vehicles or heavy machinery with BCIs are also within the realm of possibilities. A recent DARPA proposal for a “Cognitive Technology Threat Warning System” includes a requirement for operator-trained high-resolution BCI binoculars that can quickly respond to a subconsciously detected target or a threat. Such biological vision devices can have detection ranges of up to 10 km against dismounts and vehicles, and can expand soldiers' field of view to 120°.11,57 Thus, future generations of auditory and visual neuroprostheses may allow soldiers to perform better during combat situations through automated detection and interpretation capabilities.52 The concept of telepresence, in which a soldier is physically present at a base or concealed location, but has the ability to sense and interact in a removed, real-world location through a mobile BCI device, is also being actively investigated and has even been projected to be available in limited applications by 2015.1 These expectations are substantiated by recent advances in the operation of robots using EEG signals,3 such that control of cargo-loading machines, demolition robots, or unmanned aerial vehicles, as enabled by BCIs, is more than a progressive goal; it is also a realistic expectation.1,20,47 In its earliest stages, this type of BCI could be used in manned vehicles, vessels, and aircraft to make their operation more efficient by reducing the need for manual input of key functions as required by today's navigation and weapons deployment protocols.

The ethical considerations of employing BCIs for performance modification depend largely on the type of intervention required to implement the device. Because a majority of unclassified DARPA projects are based on noninvasive BCIs, use of such platforms will not be associated with additional risks and can be viewed in a similar manner as the use of night-vision goggles or radiofrequency signals. However, the application of invasive or partially invasive BCIs in soldiers presents an ethically challenging scenario that raises concerns of surgical risk as well as issues of neurocognitive enhancement and alteration of personal identity. Unlike the use of BCIs for therapeutic interventions, cognitive, physical, and psychological enhancement of healthy individuals does not fall under the principle of physician beneficence that obligates doctors to restore health to normal levels through the treatment and prevention of disease. Nevertheless, the ability of BCI devices to expand human capacities must also be viewed in light of the advantage they grant soldiers to perform and succeed in combat missions. In this context, development of BCIs can be seen as making a paramount contribution to the national security, which citizens, including physicians, have a social duty to support. Equally important is the distribution of this technology: in the hands of a responsible military, BCIs can protect national interests and the population at large, but if obtained by rogue groups, they can promote terrorism and instability. On a further level, if an existing BCI application had the potential for significant benefit in a much wider population, such as through therapeutic uses, it would be ethically questionable to sequester its use without justly distributing it to the society at large. All these and other considerations make the role of a neurosurgeon in the development of BCIs particularly complex. Nevertheless, ethical considerations must be foremost applied to the most realistic expectations, such as BCI therapeutics, and deferred in those that are presently more speculative.

Conclusions

Brain-computer interfaces and their potential applications engender great excitement. However, it must be stressed that in their present state, it remains to be seen how far, and in what direction, applications for BCIs will develop. In the near future, guided by a responsibility to the patient and civic duty, the military neurosurgeon can meet the clinical and ethical challenges presented by the field of BCIs to make optimal decisions for those who put themselves in harm's way to serve their country.

Disclosure

Brian Y. Hwang was supported by a grant from the Doris Duke Charitable Foundation. The authors report that no financial, personal, or professional conflicts of interest pertaining to this manuscript exist.

Author contributions to the study and manuscript preparation include the following. Conception and design: CP Kellner, IS Kotchetkov, BY Hwang, G Appelboom, ES Connolly. Drafting the article: IS Kotchetkov, BY Hwang, G Appelboom. Critically revising the article: CP Kellner, IS Kotchetkov, BY Hwang, G Appelboom, ES Connolly. Reviewed final version of the manuscript and approved it for submission: CP Kellner, ES Connolly. Study supervision: ES Connolly.

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Article Information

Contributor Notes

* Mr. Kotchetkov and Mr. Hwang contributed equally to this work.Address correspondence to: Christopher P. Kellner, M.D., Columbia University College of Physicians and Surgeons, The Neurological Institute of New York, 710 West 168th Street, Room 404, New York, New York 10032. email: cpk2013@columbia.edu.

© AANS, except where prohibited by US copyright law.

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Figures
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    Three classes of BCIs: their anatomical locations, advantages, and limitations.

References
  • 1

    Aliberti KBruen TL: Telepresence: harnessing the human-computer-machine interface. Army Logistician: Professional Bulletin of United States Army Logistics 38:2006. (http://www.almc.army.mil/alog/issues/NovDec06/browse.html) [Accessed March 1 2010]

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