Neuroethics in a New Era of Neuroimaging

Judy Illes

Although investigations about brain, mind, and behavior date back to the ancient philosophers, a new discipline called neuroethics has emerged formally only during the past year to embody theoretical and practical issues in the neurologic sciences that have moral and social consequences in the laboratory, in health care, and in the public domain. The first specific references to neuroethics in the literature were made a little more than a decade ago. They described, for example, the role of the neurologist as a neuroethicist faced with patient care and end-of-life decisions (1) and philosophical perspectives on the brain and the self (2). As a discipline, per se, neuroethics was launched in a conference sponsored by the Dana Foundation called “Neuroethics: Mapping the Field” held in San Francisco in May 2002 (3). Bringing together approximately 150 neuroscientists, scholars in biomedical ethics and the humanities, lawyers, public policy makers, and representatives of the media, the conference emphasized four major areas of emphasis: “Brain Science and the Self” (or “Our View of Ourselves”) devoted to issues of human freedom and responsibility, the biologic basis of personality and social behavior, choice and decision-making, and consciousness; “Brain Science and Social Policy,” including issues of personal and criminal responsibility, true and false memory, education and theories of learning, social pathology, privacy, and the prediction of future brain pathology; “Ethics and the Practice of Brain Science,” spanning topics of pharmacotherapy, surgery, stem cells, gene therapy, neuroprosthetics, and parameters for guiding research and treatment; and “Brain Science and Public Discourse,” including the development of broad and informed public discourse, mentoring of young trainees, and encouragement of responsible understanding and reporting in the media.

The ethical challenges introduced by advanced capabilities in neuroimaging were recognized as a priority for the new discipline, taking into consideration significant concerns and potentially thorny issues that have surfaced both in research and in the clinical environment. The research imaging issues are the focus of the present editorial; clinical neuroethics issues will be the focus of a forthcoming AJNR editorial.

Functional Neuroimaging: Behavior, Reasoning, Thought

In a recent report, Illes et al (4) provided empirical validation of the expanding terrain of brain imaging studies by using measurements of regional blood flow from functional MR imaging. Through an analysis of the more than 3400 peer-reviewed papers examining the application of functional MR imaging, alone or in combination with other neuroimaging modalities in the decade between 1991 (the genesis of functional MR imaging) and 2001, a steady growth in studies with evident ethical and social implications was shown. These included studies of social attitudes, human cooperation and competition, brain differences in violent people, religious experience, genetic influences, and variability in patterns of brain development.

Imagine, for example, a moral reasoning experiment in which you could choose to save the lives of five people on a runaway trolley car by pulling a switch to send it on an adjacent track where one person stands (and who would not survive) (5). Alternatively, you could choose to push one of the people off the trolley and on to the track, thereby blocking the movement of the trolley and saving the remainder of the group. Most people respond that the “switch” option is morally acceptable, while the “push” option is not (6). Functional MR imaging studies of healthy adult participants engaged in resolving such dilemmas (5), making decisions about statements that have moral content (eg, “The judge condemned the innocent man” or “The elderly are useless”) versus neutral content (“The painter used his hand as a paintbrush”) (7), or making decisions about race and stereotypes (8) have begun to probe such uniquely human processes and have pushed the envelope well beyond the lines of where neuroradiology and cognitive neuroscience have traditionally intersected.

Extending well beyond cortical maps of sensorimotor function, language, and attention, maps that include the medial frontal and orbitofrontal gyri, posterior cingulate gyrus, angular gyrus, amygdala, and fusiform area for moral reasoning, emotion and judgment—arguably among the deepest forms of human thought—have now been described. No doubt, the diagnostic and predictive validity for real-world behaviors, especially those that are potentially value-laden or culturally determined, is still unsolved (8). However, as functional MR imaging and other advanced neuroimaging technologies continue to mature, the issue of validity becomes steadily addressed (10). Therefore, with a growing regard for the novelty and breadth of information that neuroimaging can deliver about the complexity of human behavior, ethical concerns regarding the potential data misuses or abuses have come to the foreground. These range from the creation of a personal sense of stigma to discrimination in health coverage or employment.

The prima facie question for advanced neuroimaging, in fact, is moral and social acceptability of research topics and study design. We must ask, for example, whether all studies of normative neurobehavioral phenomena are ethically acceptable. How might social or racial biases affect applications of the technology, the conditions under which imaging is performed, or the way interpretations are made? What does a statistically normal activation pattern of moral behavior really mean, and, by extension, what would the implication of an abnormal brain activation pattern be in a healthy person normally (ie, within predicted behavioral or physiological norms) performing a task that involves moral judgment, deception, or even sexual responsiveness (11)? Dilemmas posed by incidental findings of structural anomalies in medical research have been raised in the past and have surfaced recently for research MR images specifically (12, 13). However, incidental findings of functional anomalies may give rise to an entirely new kind of challenge related to both the interpretation and appropriate use of data. Ensuing questions relate to what protocols may need to be put in place for the discovery of such findings and how (or if) they should be communicated to a participant (14, 15). It is imperative to consider the clinical significance of a finding, what a participant would want to know, and the risks of inadvertent disclosure or exploitive use of such information. Although one may debate whether these risks are significant, in this century marked by technological innovation and a society quick to embrace high technology, it would be imprudent to think that they do not exist at all. Just as the regulations of the new 2003 Health Insurance Portability and Accountability Act extend The Belmont Report principles and guidelines for the protection of human participants in research, what will protect the quantitation of human thought in 2010?

In 1932, Aldous Huxley wrote in Brave New World (16), “The ethical issues raised by… feats of human engineering are qualitatively no different from those we shall have to face in the future. The difference will be quantitative: in scale and rate. Even so, the individual steps may still go on being so small that none of them singly will bring those issues forcibly to light: but the sum total is likely to be tremendous. That is why we have to look for those issues now… ”

We have, in fact, entered an era in which issues surrounding the ethics of neuroimaging and the neuroimaging of ethics (ie, ethical reasoning and behavior) are now both at hand (17). Neuroradiologists have a vital role to play in identifying the issues as the new discipline of neuroethics continues to evolve and in ensuring that the enthusiasm for and benefits of neuroimaging information outweigh associated risks in any of the areas in which neuroimaging may be used practically. Knowledge harnessed from lessons of the past in genomics and other areas of biomedical research, and from the multidisciplinary perspectives of all stake holders, can provide essential information for delineating priorities for neuroimaging and ethics in research and education for the short term and for the allocation of sustainable resources and infrastructure over the long term.

Acknowledgments

The author gratefully acknowledges Dr. Scott W. Atlas, Chief of Neuroradiology, Department of Radiology, and Senior Fellow, Hoover Institution, Stanford University, for thoughtful feedback on this review, and the Greenwall Foundation for their generous support of this work.

References

↵
Cranford RE. The neurologist as ethics consultant and as a member of the institutional ethics committee: the neuroethicist. Neurol Clin 1989;7:697–713
PubMed
↵
Churchland PS, Roy DJ, Wynne BE, Old RW (eds): Our Brains, Our Selves: Reflections on Neuroethical Questions, Bioscience-Society. New York: John-Wiley and Sons;1991 :77–96
↵
Marcus SJ (ed): Neuroethics: Mapping the Field, Conference Proceedings. New York: The Dana Foundation;2002 (also available at)
↵
Illes J, Kirschen M, Gabrieli JD. From neuroimaging to neuroethics. Nat Neurosci 2003;6:205
CrossRef PubMed
↵
Greene JD, Sommerville RB, Nystrom LE, Darley JM, Cohen JD. An fMRI investigation of emotional engagement in moral judgment. Science 2001;293:2105–2108
Abstract/FREE Full Text
Helmuth L. Moral reasoning relies on emotion. Science 2001;293:1971–1972
↵
Moll J, de Oliveira-Souza R, Bramati IE, Grafman J. Functional networks in emotional moral and nonmoral social judgments. Neuroimage 2002;16:696–703
CrossRef PubMed
↵
Golby AJ, Gabrieli JD, Chiao JY, Eberhardt JL. Differential responses in the fusiform region to same-race and other-race faces. Nat Neurosci 2001;4:845–850
CrossRef PubMed
Beaulieu A. Images are not the (only) truth: brain mapping visual knowledge and iconoclasm. Sci Technol Human Values 2002;27:53–87
Abstract/FREE Full Text
↵
Desmond JE, Annabel Chen SH. Ethical issues in the clinical application of fMRI: factors affecting the validity and interpretation of activations. Brain Cogn 2002;50:482–497
CrossRef PubMed
↵
Arnow BA, Desmond JE, Banner LL, et al. Brain activation and sexual arousal in healthy heterosexual males. Brain 2002;125:1014–1023
Abstract/FREE Full Text
↵
Illes J, Desmond J, Huang LF, Raffin TA, Atlas SW. Ethical and practical considerations in managing incidental findings in functional magnetic resonance imaging. Brain Cogn 2002;50:358–365
CrossRef PubMed
↵
Kim BS, Illes J, Kaplan RT, Reiss A, Atlas SW. Incidental findings on pediatric MR images of the brain. AJNR Am J Neuroradiol 2002;23:1674–1677
Abstract/FREE Full Text
↵
Steinberg D. What information should be disclosed to patients? Medical Ethics 2002;9:1–2
↵
Kulynych J. Legal and ethical issues in neuroimaging research: human subjects protection, medical privacy, and the public communication of research results. Brain Cogn 2002;50:345–357
CrossRef PubMed
↵
Huxley A. Brave New World (1932), as cited in Stevens MLT, Bioethics in America: Origins and Cultural Politics. 2002
↵
Roskies A. Neuroethics for the new millennium. Neuron 2002;35:21–23
CrossRef PubMed

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[1] ↵
Cranford RE. The neurologist as ethics consultant and as a member of the institutional ethics committee: the neuroethicist. Neurol Clin 1989;7:697–713
PubMed

[2] ↵
Churchland PS, Roy DJ, Wynne BE, Old RW (eds): Our Brains, Our Selves: Reflections on Neuroethical Questions, Bioscience-Society. New York: John-Wiley and Sons;1991 :77–96

[3] ↵
Marcus SJ (ed): Neuroethics: Mapping the Field, Conference Proceedings. New York: The Dana Foundation;2002 (also available at)

[4] ↵
Illes J, Kirschen M, Gabrieli JD. From neuroimaging to neuroethics. Nat Neurosci 2003;6:205
CrossRef PubMed

[5] ↵
Greene JD, Sommerville RB, Nystrom LE, Darley JM, Cohen JD. An fMRI investigation of emotional engagement in moral judgment. Science 2001;293:2105–2108
Abstract/FREE Full Text

[6] Helmuth L. Moral reasoning relies on emotion. Science 2001;293:1971–1972

[7] ↵
Moll J, de Oliveira-Souza R, Bramati IE, Grafman J. Functional networks in emotional moral and nonmoral social judgments. Neuroimage 2002;16:696–703
CrossRef PubMed

[8] ↵
Golby AJ, Gabrieli JD, Chiao JY, Eberhardt JL. Differential responses in the fusiform region to same-race and other-race faces. Nat Neurosci 2001;4:845–850
CrossRef PubMed

[9] Beaulieu A. Images are not the (only) truth: brain mapping visual knowledge and iconoclasm. Sci Technol Human Values 2002;27:53–87
Abstract/FREE Full Text

[10] ↵
Desmond JE, Annabel Chen SH. Ethical issues in the clinical application of fMRI: factors affecting the validity and interpretation of activations. Brain Cogn 2002;50:482–497
CrossRef PubMed

[11] ↵
Arnow BA, Desmond JE, Banner LL, et al. Brain activation and sexual arousal in healthy heterosexual males. Brain 2002;125:1014–1023
Abstract/FREE Full Text

[12] ↵
Illes J, Desmond J, Huang LF, Raffin TA, Atlas SW. Ethical and practical considerations in managing incidental findings in functional magnetic resonance imaging. Brain Cogn 2002;50:358–365
CrossRef PubMed

[13] ↵
Kim BS, Illes J, Kaplan RT, Reiss A, Atlas SW. Incidental findings on pediatric MR images of the brain. AJNR Am J Neuroradiol 2002;23:1674–1677
Abstract/FREE Full Text

[14] ↵
Steinberg D. What information should be disclosed to patients? Medical Ethics 2002;9:1–2

[15] ↵
Kulynych J. Legal and ethical issues in neuroimaging research: human subjects protection, medical privacy, and the public communication of research results. Brain Cogn 2002;50:345–357
CrossRef PubMed

[16] ↵
Huxley A. Brave New World (1932), as cited in Stevens MLT, Bioethics in America: Origins and Cultural Politics. 2002

[17] ↵
Roskies A. Neuroethics for the new millennium. Neuron 2002;35:21–23
CrossRef PubMed

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