Ethical Issues in Brain–Computer Interface Research,
Development, and Dissemination
Rutger J. Vlek, MSc, David Steines, MSc, Dyana Szibbo, MSc, Andrea K¨ubler, Prof.,
Mary-Jane Schneider, PhD, Pim Haselager, PhD, and Femke Nijboer, PhD
The steadily growing field of brain–computer interfacing (BCI) may develop useful technologies, with a potential impact not only on individuals, but also on society as a whole. At the same time, the de-velopment of BCI presents significant ethical and legal challenges. In a workshop during the 4th International BCI meeting (Asilomar, Cal-ifornia, 2010), six panel members from various BCI laboratories and companies set out to identify and disentangle ethical issues related to BCI use in four case scenarios, which were inspired by current experi-ences in BCI laboratories. Results of the discussion are reported in this article, touching on topics such as the representation of persons with communication impairments, dealing with technological complexity and moral responsibility in multidisciplinary teams, and managing expectations, ranging from an individual user to the general public. Furthermore, we illustrate that where treatment and research interests conflict, ethical concerns arise. On the basis of the four case scenar-ios, we discuss salient, practical ethical issues that may confront any member of a typical multidisciplinary BCI team. We encourage the BCI and rehabilitation communities to engage in a dialogue, and to further identify and address pressing ethical issues as they occur in the practice of BCI research and its commercial applications. Key Words: brain–computer interface, ethics, locked-in syndrome, neuroethics
(JNPT 2012;36: 94–99)
Radboud University Nijmegen, Donders Institute for Brain, Cognition and Behaviour, The Netherlands (R.J.V., P.H.); University of Illinois, De-partment of Electrical and Computer Engineering, Urbana-Champaign, Illinois (D.St.); NeuroSky Brain-Computer Interface Technologies, San Jose, California (D.Sz.); University of W¨urzburg, Department of Psy-chology I, W¨urzburg, Germany (A.K.); Laboratory of Neural Injury and Repair, Wadsworth Center, New York State Department of Health, Albany, and Department of Health Policy, Management and Behavior, School of Public Health, University at Albany, State University of New York, Albany (M.-J.S.); and Human-Media Interaction Group, University of Twente, Enschede, The Netherlands (F.N.).
This study was supported by the BrainGain Smart Mix Programme of the Netherlands Ministry of Economic Affairs and the Netherlands Ministry of Education, Culture and Science and by the Information and Communication Technologies Coordination and Support Action “FutureBNCI” within the FP7 framework, Project Number 248320.
The authors declare no conflict of interest.
Correspondence: F. Nijboer, Human Media Interaction, Faculty of Electrical Engineering, Mathematics and Computer Science, P.O. Box 217, 7500 AE Enschede, the Netherlands; E-mail: Femke.Nijboer@utwente.nl CopyrightC 2012 Neurology Section, APTA.
ISSN: 1557-0576/12/3602-0094 DOI: 10.1097/NPT.0b013e31825064cc
INTRODUCTION
Definition
A brain–computer interface (BCI) is a system that al-lows its user to control a machine (e.g., a computer, an auto-mated wheelchair, or an artificial limb) soley with brain activity rather than the peripheral nervous system.1,2 Control with a
BCI is initiated when a user performs a specific mental task. A typical BCI combines neurophysiological measurement tech-nology with machine learning software to automatically detect patterns of brain activity that relate to this specific mental task. In most BCIs, the user is provided with a small selection of mental tasks (e.g., imagined movement of left hand, right hand, or foot) that the system is trained to detect. Once the system detects that the user has been performing one of the mental tasks, the corresponding actions are automatically triggered (e.g., move cursor left, move cursor right, or click cursor). The following subsections will provide a short overview of relevant aspects of the technology and current state of the art, leading up to the discussion of ethical aspects.
Measurement Techniques
Implementation of a BCI requires brain activity to be measured. Technology to do so can be categorized as either invasive, such as subdural or epidural electrocorticography or implantation of a multielectrode array, or noninvasive, such as electroencephalography (EEG), magnetoencephalography, functional magnetic resonance imaging, or near-infrared spec-troscopy. All of these technologies provide some representa-tion of the brain’s activity. The choice of a specific method is often determined by a balance between factors such as health risks, user comfort, signal quality, portability, and cost. “Wet” EEG, which involves the use of conductive gel to improve the electrode’s connection to the surface of the scalp, is still the most popular noninvasive method for clinical BCI appli-cations. However, low-cost wireless and “dry” alternatives are emerging rapidly, often aimed at less-critical consumer ap-plications, such as BCI games and entertainment for healthy users. BCI technology brings many promising applications in a variety of clinical and nonclinical areas. However, at present, clinical success with BCI is predominantly achieved with pro-totypes in research laboratories.
Applications
Clinical applications of BCI can be roughly divided into two categories. The first category aims at providing a
technological alternative for a user’s lost function and can be considered a form of assistive technology. The second cate-gory aims at rehabilitation of the user’s own neural pathways to restore the lost function (see also Daly and Wolpaw3).
In the category of assistive technology, invasive BCI sys-tems have been reported as specialized at real-time decoding of motor functions in nonhuman primates, sometimes even re-producing the decoded motor activity with a cursor or robotic arm.4-6 Eventually, such technology may develop into neu-romotor prostheses for humans with motor disabilities. One successful case has been reported in which neural cursor con-trol was achieved by a person with tetraplegia, who had a multielectrode array implanted in the motor cortex.7
Noninvasive BCI systems, mostly EEG-based, have also been investigated for various assistive applications, of which one of the most popular is communication. Spelling applica-tions, for instance, relying on the so-called P300 response, enable a user to “mentally type” symbols on a screen by fo-cusing on specific symbols in a matrix of randomly flashing symbols (usually letters, punctuation marks, and numbers).8,9 Variations of this application have also been presented for use in the auditory domain,10which may be relevant to users with
a progressive neurodegenerative disease affecting vision in its later stages (e.g., amyotrophic lateral sclerosis [ALS]). One of the key problems in these types of communication applica-tions is speed. To achieve sufficient reliability of the system, repeated measurement of the P300 response is necessary, re-sulting in reduced speed of the application.11 Attempts have
been made to overcome this lack of speed by adding artifi-cial intelligence to the application in the form of automatic word completion or error correction from a dictionary (see, for instance, Ahi et al.12), or even entire graph-based sentence
databases (such as described in Geuze et al.13). This increases
throughput of language at the cost of verbal freedom. In addi-tion to communicaaddi-tion applicaaddi-tions, prototypes for wheelchair control14or three-dimensional cursor control15have also been reported.
In the category of applications for rehabilitation, var-ious results have been reported with the use of an invasive or noninvasive BCI for rehabilitation of gait after stroke.16-18
In these applications, attempted or imagined movement is de-tected by a BCI and used to artificially move the user’s limb with a robotic aid or by functional electrical stimulation of the muscles. This movement provides the user with proprio-ceptive and visual feedback of the limb following his or her intention, which, in turn, stimulates neural plasticity and then allows the user’s own neural pathways to regain control of the limb. Furthermore, BCI is being investigated as a therapy for various cognitive disorders. This is typically done by feeding back functional magnetic resonance imaging measurements to subjects in real time, allowing them to self-regulate a specified area of the brain. Initial studies have illustrated a wide vari-ety of potential applications in treatment of pain, depression, schizophrenia, tinnitus, emotional disorders, and memory.19-21
Besides current and potential clinical applications of BCI, applications are also being developed for game and enter-tainment purposes.22Because of the large number of potential users of such applications, this likely will increase research and development resources, from which clinical applications may
benefit as a side effect. Moreover, recent work by M¨unssinger et al.23on a BCI painting application illustrated that even enter-tainment BCIs may have a certain degree of clinical relevance by improving the user’s social and expressive potential.
Present Research and Development Issues
The fact that BCI technology for clinical use, although promising, still resides predominantly in research laboratories can be explained by several factors. A key factor is the so-called signal-to-noise ratio in a given measurement modality, where the definition of noise includes any signal (including brain signal) that is not of interest to the discrimination of responses to the specific mental tasks used to control the BCI. Both speed and reliability of a BCI system are dependent on this signal-to-noise ratio. In addition, the signal of interest typically varies greatly among and within subjects over time. This makes the quality of a BCI for a specific individual at a specific time very difficult to predict and may lead to frustration for the user when the BCI suddenly stops working. It also means that most BCI systems require training or adjustment to each subject individually. Finally, artifacts may be contribute to initial success with a prototype but to a difficult transition into clinical applications. Especially with EEG-based BCIs, signals originating from sources other than the brain, such as eye movement and muscle activity, may (sometimes without being noticed) boost BCI performance. When the transition is made from healthy users (which is typically the first group to try a prototype) to persons with disability, some of the performance previously achieved may be lost as a consequence of physical conditions. Much of the ongoing BCI research is focused at finding solutions for the issues described previously.
Ethical Aspects
In the future, BCI has the potential to impact not only individual users but also society as a whole. The research and development of future BCI applications such as BCI computer games, neuroprostheses, online cognitive research, neuromar-keting, or cognitive enhancement2inevitably raise ethical and
societal challenges, and a public debate on rights and restric-tions is to be expected. Apart from being important in their own right, these ethical debates may substantially influence public acceptance of BCIs and related neurotechnologies.
Nascent neuroethical debates have identified several top-ics of importance to BCI research, development, and dissemi-nation (see Clausen,24Haselager et al.,25Tamburrini,26 Tam-burrini and Mattia,27Fenton and Alpert,28and Walter29). Some
of the ethical issues are well known in medical research and the medical device industry. However, there is also a category of issues that are relatively unique to BCI research. Some issues such as the complicated process of obtaining informed consent from persons with locked-in syndrome (LIS) can readily be identified,24 whereas other issues may be less obvious or con-crete (e.g., privacy and mind-reading). One basic distinction that permeates ethical debates on BCI concerns the difference between research and treatment. Ethical issues depend, at least in part, on whether the aim is to apply approved technologies for treatment or to develop technologies. Especially in cases where treatment and research interests conflict, important eth-ical concerns can arise (see the “Jane” case scenario below).
In an effort to triage issues according to technological imminence and ethical novelty,30we set out to identify and dis-entangle ethical issues related to BCI use in four case scenarios that were inspired by current experiences in BCI laboratories. Six panel members from various BCI laboratories and compa-nies discussed each case scenario in the workshop on “Ethical Issues in BCI Research, Development, and Dissemination,” which took place at the 4th International BCI Meeting (Asilo-mar, California, 2010). Results of the discussion are reported in this article.
We have chosen to discuss ethical issues, driven by the case scenarios, in an attempt to illustrate how issues relating to moral responsibility can, in different ways, confront re-searchers, clinicians, and developers with backgrounds in any of the various disciplines typically involved in BCI research or application. Because the case scenarios are related to issues confronting BCI teams now (cases 1–3) and potentially in the near future (case 4), they may also provide challenging ma-terial for analysis by those interested in the more theoretical ethical debate on neurotechnologies (such as BCI and deep brain stimulation).
CASE SCENARIOS
“Jane”
Jane is a 46-year-old housewife who has had the neu-rodegenerative disease ALS for 10 years. She lives at home and has a full-time staff of caregivers. Since the onset of locked-in syndrome 1 year ago, she has not been able to communicate in any way. She has a legal representative who enrolled her in tests with noninvasive brain-computer interfaces. The re-searchers using noninvasive BCI say they can see that Jane is making an effort but that they are unable to reliably decode Jane’s brain activity. Jane’s husband, who is eager to commu-nicate with his wife again, has read about invasive BCIs in the media and would like to try this method. He asks the BCI team whether his wife could be considered for brain surgery.
Jane’s case illustrates BCI research with the most vul-nerable participants, namely those who cannot communicate. In such situations, a surrogate decision maker or legal repre-sentative is needed to represent the participant. Ethics in this regard are partially codified by law. There are different inter-national regulations specifying when a person is considered to be legally incompetent and who should then be the legal rep-resentative. In the United States and the Netherlands, a close relative is a preferred representative, whereas in Germany the preferred representative is a neutral person. Such differences between countries prevent a straightforward global discussion of the ethical aspects of BCI. Other legal issues include the liability of research teams. Currently, initiatives are under way to systematically gather information about international legal practices in relation to neuroscience and neurotechnologies (see, for example, Nadelhoffer31). Furthermore, depending on
national legislation, a conflict of interest may occur when close relatives legally represent a person who is unable to com-municate. Caregivers and family members tend to underesti-mate the quality of life of persons with disability32 and may choose not to let their loved one “endure” additional BCI train-ing. Alternatively, caregivers and family members may be so
desperate to communicate with their loved one that they would accept just about any intervention offered to them.
The second topic raised in Jane’s case is how a BCI team should reply to the request from the husband of a person with complete locked-in syndrome (CLIS) to try a BCI interven-tion, assuming that the legal representative (if this is not the husband himself) also shows an interest in the BCI interven-tion. It is common for BCI research laboratories to receive such requests for intervention from people (when not yet CLIS) or from their legal representatives. Researchers may also have an interest in working with persons with CLIS, for example, for understanding commonalities and differences between healthy user groups and user groups with disabilities, thus creating a situation of mutual interest between potential user or repre-sentative and researcher. Despite their mutual interest, both parties often do not share the same goal. Motivation from a research perspective can conflict with a therapeutic interest, sometimes leading to a “therapeutic misconception” of the subjects participating in the research. Subjects then “fail to distinguish between clinical care and research and to under-stand the purpose and aim of research, thereby misconceiving their participation as therapeutic in nature.”33When research
is confused with therapy, the participants or their legal rep-resentatives might fail to make decisions that are in the best interests of the participants; in addition, researchers might not adequately understand the motives of their participants.
From a broader perspective, there is also another ethi-cal aspect to BCI treatment and research. At present, any BCI intervention would draw from scientific resources, for which responsibility lies with the researcher or the research group. A moral aspect of this responsibility yields a balancing act be-tween the freedom and well-being of the individual versus that of the public. Because of typical interindividual differences between BCI users, resources spent on improving a system for a single user do not necessarily improve BCI for other users, whether these are individuals in the same disability group or in any of the other potential BCI target groups. Moreover, the balance between individual and public welfare may be skewed if pressure is put on access to experimental assistive technology by users who face the prospect of communica-tion impairments or physical disabilities. A similar pressure was observed regarding experimental medication for acquired immunodeficiency syndrome, which led to public debate and lawsuits concerning the public right to experimental treatment (see, for example, Richman34and Leonard35).
“Nigel”
Nigel is a 51-year-old research scientist who has had ALS for 11 years. He has used a P300 BCI home system for 4 years to communicate with his family members and for professional purposes with his laboratory colleagues. In recent months, he has dramatically reduced his use of the system and appears to be losing the capability to control it. The BCI team has noticed the decline and is trying hard to determine whether the algorithms need to be adapted.
Unlike the first case scenario, Nigel is able to commu-nicate. Persons with LIS like Nigel may also have a legal representative who must give the legally necessary informed consent. In addition, a person with LIS may still be able to give
assent. Where this is possible, even by only signaling “yes” via eye blinks or other muscle twitches, researchers must seek that assent in addition to the consent of the legal representative, and dissent should be respected.25,36
Second, the information regarding what to expect from a BCI system is crucial for giving informed consent. In this case scenario, the subject should have been informed about a possible decline in BCI performance, but managing expecta-tions of a BCI proves to be difficult. Although a BCI system, in principle, yields numerous useful applications for a user, factors such as intersubject differences and the brain’s plas-ticity make it hard to predict BCI success for a specific user. The multidisciplinary nature and typical size of a BCI research team contributes to this problem. Various members of a team may assess expectations of a system differently. Haselager et al25point out the similarity with other interdisciplinary teams
working in similarly demanding situations, such as intensive care or mental health care. Furthermore, BCI performance may be related to physical decline.37 If this is the case, informing
the user with disability about BCI expectations implies that information is also provided regarding progress of the disease, which the person may not (yet) want to know about.38Finally,
overly enthusiastic media coverage about BCIs could heighten an individual’s expectations of BCI, further undermining in-formed consent.39
A third issue that arises when visiting persons with se-vere paralysis or locked-in syndrome at home is that BCI training inevitably interferes with their care and daily life (and the lives of their family and/or caregivers). This is a factor that researchers should include in moral considerations. For exam-ple, a person with LIS who has phantom limb pain reduced her morphine intake on days when she was training with a P300 BCI, because she knew that morphine could reduce de-tection of the P300. Participants may opt to accept discomfort, changes in care schedules, or even pain to be able to work with the BCI. For this reason, the interference of BCI with daily life and care is a potential ethical concern. Information about the extent of interference with daily life is crucial for weighing positive and negative effects in making decisions about BCI intervention. Participants in BCI studies often report feeling positively challenged by training. For example, subject H., who participated over 2 years in three BCI studies, stated that he looked forward to every training session, because he knew he could “work with his head” and that he was mentally as healthy as other people.40A recent study showed that most participants were highly motivated throughout BCI training and their mood was often good before training.41
“Ben”
Nine months ago Ben had a stroke, resulting in paral-ysis of his right arm. He has regained some function in his arm after months of extensive motor rehabilitation, and Ben’s doctor asked him to enroll in a study that investigates whether BCI neurofeedback could accelerate Ben’s recovery. Ben has difficulty understanding what the doctor is asking of him (he has minor cognitive impairment), but he trusts his doctor.
Ben’s case refers to more recent BCI studies, which in-vestigated the effects of neurofeedback training on the rehabili-tation process after stroke.3,16,42-44The combination of acutely
ill and vulnerable participants demands an especially careful evaluation of risk and benefit, the process of consent, and the permissible treatment of control participants.45 The question
could be raised whether Ben, given his cognitive impairment, is really the most suitable subject for the study. In this situ-ation, merely presenting Ben the option of BCI intervention may already carry some coercive weight. The issue of coer-cion is not unique to BCI and has been empirically addressed in the literature.46Furthermore, this case emphasizes the need for clear inclusion and exclusion criteria for any study to be performed with participants in possible need of BCI.
A second issue relates to possible side effects of BCI intervention and, more specifically, neurofeedback training. No adverse side effects of BCI intervention and training have been reported, but no systematic research exists on this topic. Some BCI teams exclude study participants with epilepsy, which may be of relevance in studies involving flickering vi-sual stimuli at specific frequencies and high contrasts, such as the stimuli sometimes used to evoke a P300 or SSVEP (steady-state visual evoked potential) response. In a neurofeedback study, Hoedlmoser et al.47 noted an impact of sensorimotor
rhythm training on sleep and declarative learning. Their train-ing paradigm is very similar to a paradigm regularly used in the BCI community.48,49Regarding the use of the brain’s plasticity
for obtaining or improving BCI control or rehabilitation, one of the panel members remarked that if we can do any good, we can certainly also do harm. The question here is: how different is mental training in BCI from any other forms of training with which we are already very familiar (e.g., driver training or sub-ject preparations for psychological experiments), and are any of these differences cause for ethical concern? We recommend that in future clinical trials all positive and adverse side effects be systematically investigated.
Beyond rehabilitation of gait after stroke, the princi-ple of neurofeedback or self-regulation is being investigated for treatment of various neurological or cognitive disorders, as discussed in the introduction to this report. The increas-ing number of potential applications in this therapeutical area brings us into a different domain of ethical questions, regard-ing identity and change of personality and self-perception.26,50
When, for instance, BCI is used for rehabilitation of an emo-tional disorder, one could wonder how this affects personality, albeit as a side effect or as the main effect. A similar type of neurotechnology that is currently being investigated for a variety of diseases such as psychiatric disorders, Alzheimer’s, and Parkinson’s disease is deep brain stimulation. The ethi-cal debate surrounding deep brain stimulation technology is addressing similar issues of identity and personality.51,52
“Thomas”
Thomas is a 30-year-old air traffic controller who was told by his boss that starting this month he would have to un-dergo attention training by wearing a new neurotechnological tool that provides him with neurofeedback. Thomas does not know exactly what the device does, but he feels that his at-tention has somewhat improved since he started training. The explanation that Thomas was given about the new tool was that it somehow reads his brain, so he is sometimes afraid the tool can also read his thoughts. Also, last Monday Thomas got
a lecture from his boss, who said he could see that Thomas most likely had been drinking alcohol on Sunday night.
The scenario of Thomas (albeit somewhat futuristic) touches upon more philosophical topics such as extended28 and enacted mind,29but most importantly it raises concern for
mind reading and privacy. As this case scenario illustrates, em-ployers may be able to gain more information than had been agreed upon when they require an employee to use a BCI sys-tem. Furthermore, the subject may be completely unaware of the extent of information that is being obtained from his or her brain.
In this case, the employer was able to discern the fact that the subject might have been drinking the night before, but more generally a BCI system may be able to reveal other psy-chological states, traits, and mental health vulnerabilities.53It
may not be in an individual’s best interest to have this personal information available to others, especially an employer, and workplace discrimination could be a concern. It could be seen as a violation of a person’s right to privacy. Furthermore, the case scenario raises concerns about social stratification and brain enhancement.54,55 If brain enhancement does become
effective and popular, there could be pressure to enhance one’s brain to keep up with the competition. Barriers such as cost could prevent some people from accessing this enhancement. This issue, though complicated, is not unique to BCI and is further discussed elsewhere.25,26,30,53
SUMMARY
BCI may lead to useful technologies for humankind but at the same time present significant ethical and legal chal-lenges. The challenges are due to several factors: BCI is a rapidly growing research area with potential future applica-tions of great daily significance, for both medical and regular users, that is bound to attract the attention of media and com-mercial enterprises.
In the four case scenarios, we have identified ethical issues related to the application of BCI for users with disabil-ities and healthy users. Issues typical to the field of BCI relate to working with sensitive user groups, dealing with techno-logical complexity, and handling multidisciplinary teams. We illustrated that when treatment and research interests conflict, ethical concerns arise. Managing the expectations of this novel technology is important on different levels, ranging from indi-vidual users to legal representatives to the public (via the me-dia). We encourage researchers to facilitate ethical and public debate and keep expectations in line with achievements, be-cause the future success of both BCI research and commercial applications will rely on public acceptance of the technology.
Practical recommendations from the panel members consist of creating more awareness of ethical aspects in the BCI field, which involves reaching members of all disciplines in a typical BCI multidisciplinary team. To facilitate discus-sion and sharing of information on ethics, we recommend the organization of an ethics workshop or discussion group in fu-ture field-specific conferences. Moreover, we suggest inviting ethicists and philosophers to participate in this dialogue. We hope that these recommendations, as well as this report, will contribute to the ability to identify and address pressing ethical
issues as they appear in the rapidly progressing BCI research and commercialization.
ACKNOWLEDGMENTS
The authors thank Jonathan Wolpaw and Leigh Hochberg.
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