Neuroethics is the area of bioethics that focuses on issues unique or especially relevant to neuroscience. It is a relatively new term that has been used in a variety of more restricted ways referring to: (1) ethical issues associated with neurology (the subfield of medicine focused on disease and injury of the nervous system) (Pontius 1993); (2) ethical issues associated with the technological advances of neuroscience (Farah and Wolpe 2004); and (3) the neurological basis of ethical thought and behavior (Caplan 1983, Roskies 2002). While attention has primarily focused on the potential applications of technological development, all of these topics appropriately fall under the purview of neuroethics.
Neuroscience is that field of the biological sciences that examines the structure and function of the nervous system. It includes all stages of development from initial differentiation of cells that will become part of the nervous system in the developing organism, through senility and brain death. Topics of investigation range from the submicroscopic level, that is, ions and molecules that are involved in nerve cell function and the genes that are uniquely expressed in the brain, to mental activity and behavior. It includes, but is not limited to, the fields of neurochemistry, neurophysiology, neuropharmacology, neuroanatomy, neuroendocrinology, psychoneuroimmunology, neurology, psychiatry, psychology, and cognitive science.
Neuroscience, directly or indirectly, examines the underpinnings of thought, feeling, and behavior. Neuroethics is concerned with ethical, legal, social and or public policy implications of neuroscience research findings, as well as with the character of the research itself. The neurosciences are rapidly evolving and advances in science and technology have made possible ever more detailed examination of the nervous system and its activity, and of behavior and mental processes. As a result, what were once merely hypothetical situations and potential ethical issues and concerns are increasingly more real and immediate.
The term neuroethics seems to have first been coined in 1993 (Pontius 1993), though widespread usage of the term followed a seminal conference in 2002 (Marcus 2002). However the concept has a long history: The tension between notions of free will and determinism and the seeming duality of the mind and body have been of substantial interest to ancient as well as modern philosophers and increasingly among neuroscientists themselves. In the 1950s and before, concerns associated with prefrontal lobotomy and brainwashing as techniques for altering or influencing brain function received increasing attention (Valenstein 1986). In the 1960s some proposed psychosurgery as a method of social control, which created considerable controversy (Chorover 1979, Valenstein 1980). Beginning in 1983 the Society for Neuroscience, the primary professional society of neuroscientists in the United States, initiated annual social issues roundtables aimed at examining the ethical, legal, and social implications of neuroscience research. These symposia examine a wide array of topics including research into possible sex differences in the brain and the application of that research, therapeutic and nontherapeutic use of cognitive enhancers, neurotoxicity of food additives, brain death, the use of fetal tissue to treat neurological diseases, and the role of neuroscience research into drug addiction in the development of health and public policy. In 1983, the Office of Technology Assessment (OTA, a former congressional agency whose mission was to provide legislators with information about scientific findings relevant to the development of public policy) commissioned a report on the societal impacts of neuroscience (OTA 1984). Thus while the term neuroethics is relatively new, the field that it names is not. Rather it is a long-standing area of interest given new life with a new name and new tools.
Features of the Nervous System
Four characteristics of the nervous system with important implications for neuroethics are (1) its complexity, (2) its plasticity, (3) the dynamic, interactive quality of its elements, and (4) the remarkable variation in structure and function from one individual to the next. Although the brain is widely thought of as an organ of the body analogous to the heart, kidney, or liver, the brain and associated elements of the nervous system are more complex than the rest of the body. More genes are uniquely expressed in the brain (Hahn, Van Ness, and Chaudhari 1982) and more different types of cells are found in the brain than in the rest of the body. In addition, cells are interconnected, sending and receiving electrical and biochemical communications from nearby cells as well as cells in distant parts of the brain and the body. As a result, cell circuits extend the complexity of the brain.
The nervous system is remarkably adaptive. The interconnectivity of the cells of all components of the nervous system including the brain and sense organs, (and indeed connections with the endocrine, immune, and other physiological systems) lead to dynamic, interactive communication that makes it possible for brain cells to be sensitive to, and responsive to, changes both internally within the organism, and in its external environment. The interactive communication between cells also results in short-term and sometimes long-term changes in the cells themselves that, for example, may make the individual organism more, or less, responsive to a particular external stimulus.
Technological advances reveal increasingly detailed information about molecular and cellular mechanisms of perception, emotion, cognitive function and behavior. At the same time, the complexity and adaptive nature of the nervous system result in a certain fluidity of information about the brain. Theories of brain structure and function continue to evolve and however much is known, much remains to be discovered.
The concerns that are encompassed in the domain of neuroethics are associated uniquely or especially with the practice or conduct of neuroscience research or with the application of neuroscience findings.
CONDUCTING NEUROSCIENCE RESEARCH. All areas of research share some ethical issues associated with the nature of research itself. Integrity of the research process affecting reliability of results, appropriate allocation of credit, and management of potentially conflicting interests are among the many issues that are common to all areas of research to one degree or another, and do not fall exclusively into the purview of neuroethics. However even topics that are common to many fields, such as the humane treatment of research subjects and controlling for bias in research design, have special relevance to research in the neurosciences.
As an example, one of the ethical principles fundamental to research involving humans is respect for persons and its corollaries of autonomy and informed consent or decision making. Among the implications of these principles are that individuals must voluntarily choose to participate in research (i.e., they cannot be coerced, deceived, or manipulated into participating), and that they can discontinue their involvement at any time during the research. One broad area of neuroscience research explores the causes and mechanisms that underlie dementia, including Alzheimer's disease, with a primary long-term goal of developing treatments and a cure. Participation or involvement of individuals with early symptoms can be invaluable to various lines of research into any disease. However the capacity of ill individuals, even those who are healthcare professionals, to make a fully informed decision to participate in research is debatable. Moreover unlike most ill individuals, for example those with heart disease, patients with dementia may have a diminished capacity to fully comprehend the ramifications of consent to research participation depending upon the extent of their disease. As an example, agreement to provide a monthly blood sample may seem less onerous when an individual can comprehend an altruistic goal of developing a cure for Alzheimer's disease. As the disease progresses the individuals understanding of the research may become little more than the awareness of a painful needle. While the clinical research community has developed proxy or surrogate consent as a strategy that allows family members or other legal guardians to give consent for the patient, the notion of research participation as a fully informed choice becomes questionable and problematic.
Neuroscience research with laboratory animals also poses special concerns. Required for both the ethical and scientific justification of the use of laboratory animals in research is that the work has the potential to provide valuable insights into biological structure and/or function that lay the foundation for the understanding, and ultimately treatment, prevention, and/or cure of disease. The companion expectation is that research with animals can be carried out with minimal or no pain, suffering, or distress to the animals. Some areas of neuroscience research challenge these two concepts. For example, when research focuses on mental conditions like schizophrenia or elements of cognition like intentionality, investigators must make assumptions about the similarity between the brain activity of laboratory animals and humans. The reliability of those assumptions and their implications for the understanding of human brain function and disease can be questioned. Moreover when the focus of research is pain or stress, then pain and/or stress are unavoidable elements of the research itself. Indeed, paradoxically, the more like humans a research animal is, the more informative is the research yet, one could argue, the less reasonable the justification for conducting the research in animals because it is unethical to investigate the phenomenon in humans. Institutional Animal Care and Use Committees (IACUCs), in particular, and, to a lesser degree, the peer review process consider the ethical issues associated with the use of animals in research. However the special problems posed by neuroscience research may not always be explicitly or fully considered.
Controlling for bias in research design, while always an important aspect of research ethics, is of particular relevance and concern in neuroscience research because of the extent, nature, and implications of findings in this field. Assumptions that underlie research questions may not be adequately investigated themselves. Yet they are likely to reflect conscious or unconscious bias that arises from long-standing socially determined beliefs. For example, it is widely assumed that some differences in male and female behavior reflect anatomical and physiological differences in the brains of males and females. While this may be true, it is not clear whether biological differences relevant to behavior result from the presence of different sex-related genes or molecules, or from differences in the myriad external factors that shape interactions with others from birth, or a combination of both. Whatever the basis of sex differences in behavior, the extent to which they are linked to biology and perceived as predetermined and immutable can have far-reaching ramifications for education, employment, healthcare, and other areas of social and public policy.
APPLICATION OF RESEARCH FINDINGS. The ethical issues associated with the use of research findings are linked to the particular application: Who uses the information, how is used (e.g., to monitor brain activity, to manipulate behavior, etc.), and for what purpose (e.g., therapy, enhancement, etc.). In addition, whether the information is about the general population or about a particular individual, the accuracy and reliability of the information is always an important consideration, as is accurate presentation of its limits because it directly affects the capacity of individuals to make informed decisions.
Individuals may seek information for self-knowledge, therapy, or self-enhancement. If the information is general and benign, with noninvasive applications (e.g., mnemonic techniques for remembering names) the accuracy and reliability of the research findings are less critical than if the information may expose an individual to risk (e.g., research that suggests a particular dietary supplement is an effective sleep aid although it has the potential for inducing heart arrhythmias). When research findings provide information specific to a particular individual, the accuracy and reliability of the information is critically important depending on the nature of the information and the purpose for which it is being gathered. Thus the reliability of predictions of a test for a debilitating hereditary neurological or mental illness is key. If test findings are perceived to be consistent indicators (markers) for the disease (i.e., individuals with a positive test result inevitably get the disease), then the actual reliability and limits of the test (and the research upon which the test is based) are critically important so that individuals being tested can make adequately informed medical and personal decisions. At the other end of the continuum, if the test is an indication of a predisposition for a mental illness (a much more common occurrence), then additional ethical concerns arise.
In particular, given the dynamic and interactive nature of the human mind, knowledge of the identification of a biological element that is neither necessary nor sufficient for a mental illness but rather indicates a predisposition for that condition can become a contributing factor in its own right, and a self-fulfilling prophecy. Thus ethical concerns regarding information about predispositions to disease are related not only to the accuracy and reliability of the test, but also to the nature of the nervous system and the independent power of the information itself. In addition, given the continuing social stigma associated with mental illness, provision of test results to third parties, whether health insurance providers, employers, family members, or others, may also contribute to stress and the development, expression, and manifestation of disease. As a result, information about mental function poses risks as well as benefits because it is provided in a personal and social context with which it interacts. Technological advances can improve the accuracy of the information but may not have much impact on the contexts in which it is provided.
When neuroscience research yields scientific information and technological developments that make possible access to the brain activity of others, additional ethical concerns arise. Fundamental to this is the actual and perceived correlation between brain activity and mental activity. The possibility of monitoring the mental activity of others raises concerns about privacy and notions of individual integrity. In general, respect for the individual includes the right to privacy and exceptions are only allowed when the health, safety, and welfare of that individual, or others, is threatened. The extent of the invasion of privacy (and attendant harm to the principle of respect for persons and potential harm to that individual) is balanced against the seriousness and certainty of the harm or threat to be averted. An obvious setting in which such privacy might be invaded is in the criminal justice system. It is well-established that eyewitness testimony is unreliable. The potential for conflicting interests among experts as well as the concerns of a hostile or threatened witness can also call into question the reliability of courtroom testimony. Thus, if and when it is possible and in the putative interest of justice, authorities might seek to access directly the memories of a witness or an accused to determine what actually happened. Similarly they might seek access to the mental activity of a perpetrator in order to determine the individual's intentions.
Increasingly, advances in technology also make possible direct intervention in brain function in an even more nuanced and refined way. In the mid- to late-twentieth century, brainwashing, electroconvulsive shock therapy (ECT), and psychosurgery were used to alter brain function and behavior. These procedures are relatively crude and invasive. Current psychosurgery methods, referred to as stereotaxic surgeries, use heat or radiation to destroy very specific tissue identified using brain imaging techniques. Compared to earlier forms of psychosurgery (also known as functional neurosurgery for psychiatric disorders), such as prefrontal lobotomy, stereotaxic surgeries are relatively less invasive, success rates are high, and complications are minimal. Nevertheless the procedures are irreversible, and surgeries (and electroconvulsive shock therapy) are employed in therapy only as a last resort for treating serious mental illness that has not responded to other forms of treatment.
With increased understanding of brain chemistry, physiology, and pharmacology has come the development of pharmacological agents targeted to particular biochemical pathways because research indicates that the neurotransmitter systems associated with these pathways are associated with particular mental activity. These pharmacological agents are primarily designed to be prescribed to treat an individual's self-report of dysfunction. Issues of benefit versus risk, patient expectations and informed decision making, and allocation of resources are ethical issues that arise with any therapy. However because brain dysfunction and mental illness are often at the extreme ends of normal brain function, some therapeutic agents may be able to enhance normal function. For example, some treatments for Alzheimer's disease or other forms of dementia may be able to enhance normal cognitive function. The use of pharmaceuticals for nontherapeutic enhancement rather than therapy not only changes the benefit versus risk analysis, and alters discussions of the fair allocation of scarce resources, but also raises questions regarding who is being enhanced, by whom, and for what purpose.
Computer Brain Interfaces. In the early twenty-first century research is exploring the possibility of electrochemical implants that can serve as a brain computer interface (BCI). These, too, are initially designed to be therapeutic (e.g., to overcome physical limitations or visual deficits). However there is a distinct and important difference between the BCI that makes the brain of a quadriplegic a transmitter that can manipulate the external environment (e.g., move a cursor on a computer screen) and an implant that makes the brain a receiver either for information about the outside world or for altering brain function (e.g., to treat obsessive-compulsive disorder).
While manipulation and control of others are always ethically problematic because they violate the basic bioethical principle of respect for individuals and their autonomy, two primary considerations are (a) the degree of invasiveness and (b) the extent to which the individual being controlled is aware of, and consents to, the control (Dworkin 1976). The degree of invasiveness is a fluid notion since education and subliminal suggestion while not physically invasive like pharmaceuticals and BCIs can permeate one's thinking with long-term, widespread effect (e.g., educational programs that include evolutionary theory and/or creationism or that exclude reference to or acknowledgment of the Jewish holocaust and/or Chinese comfort women). Moreover the conscious intent of manipulation or control may well be in the eye of the beholder. Thus education while not physically invasive is potentially manipulative, subliminal suggestion is not physically invasive but is designed to be manipulative, and psychoactive agents and BCIs are invasive but can be perceived as manipulative or not. Scientific and technological advances that reflect new or refined understanding of brain structure and function have the potential for making possible more specifically targeted monitoring and manipulation of individual or group perceptions and function, but the ethical concerns are akin to those raised regarding con artists, rabble rousers, propaganda, and deceptive advertising.
Issues of Self-Knowledge. More complicated are the ethical issues associated with the scientific and technological advances in neuroscience that make possible increased nontherapeutic self-knowledge, modification, and enhancement. While insights into one's own motivation, self-understanding, personal growth, and development are generally lauded, artificial means for obtaining such insights, for example, through psychoactive recreational drugs, is often frowned on primarily because of the potential risks associated with psychoactive drugs and their uncertain benefits. Yet it is possible that techniques in brain imaging may reveal individual traits or thought patterns similar to (or different from) those revealed by less scientifically or technologically dependent approaches (e.g., psychotherapy, meditation, or prayer). Psychotherapeutic agents that modify brain chemistry to treat mental conditions (e.g., anxiety, depression, or schizophrenia) are prescribed, and taken, to modify brain function, mental activity, and behavior. Individuals taking these agents may feel more like themselves or conversely not themselves. This not only prompts the philosophically interesting question of how one defines and recognizes the self, but also raises ethical concerns regarding the extent to which peer and/or societal pressures may lead an individual to modify his or her mental processes, behavior, or other elements of the self in order to conform to the expectations of others or to internalized social norms. In addition, artificial enhancement of performance, whether mental or physical, is highly controversial, and the potential development of cognitive and/or emotional enhancers to gain personal advantage raises issues of respect for persons (i.e., the self and others) and informed-decision making, risk versus benefit, the fair allocation of resources, and fairness in competition.
Neurobiology of Ethics
The other side of the conceptual coin of neuroethics is the neurobiological underpinnings of ethical thought and practice (Caplan 1983, Roskies 2002). The cognitive and emotional elements that contribute to ethical reasoning and behavior are relatively unexamined. Nevertheless ongoing and future neuroscience research is likely to contribute to an intellectual understanding of moral development, the processes of moral reasoning and decision making, and the mechanisms by which ethical decisions are expressed in behavior. How society understands notions of free will and moral agency will be influenced by the findings of neuroscience research. Of necessity this understanding will reflect recognition of the limits of human capabilities: "it simply makes no sense to talk about ethical ideals that are beyond the reach of human conduct, motivation and behavior" (Caplan 1983, p. 106).
However a potential pitfall, as with research in neuroscience in general, is the way that conscious and unconscious assumptions may introduce an inappropriate bias into research design, analysis, or reporting. For example, it is widely assumed that moral reasoning is a rational rather than emotional process. This assumes a potentially false dichotomy in brain processing. Thus the ethical issues that are likely to be raised by future investigations of the neurobiological basis of ethics will be complex and dynamic like the nervous system itself.
As suggested, a critical element in identifying and examining some ethical issues associated with neuroscience hinges on the relationship between brain activity and mental activity. While the consensus of the neuroscience community is that, at least in humans, brain and mind are two sides of the same coin, there is considerable controversy and disagreement regarding the degree to which mental activity can be correlated with, identified as, and reduced to brain activity. An early notion was that each individual memory was embodied in a single cell so that, for example, every individual has a specific cell dedicated to his or her grandmother (hence the name grandmother cell theory). That particular concept of memory has been discredited. Moreover, the view that patterns of brain activity detectable with imaging technologies or by monitoring electrical changes can be identified with specific cognitive functions is not universally accepted. The reliability of this correlation is central to the ethical concerns associated with the scientific and technical developments in neuroscience.
There is much more to be learned about the structure and function of the nervous system. It is clear that the ethical issues inherent in the practice, applications, and implications of this area of research will continue to become apparent.
STEPHANIE J. BIRD
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