Imaging or Imagining? A Neuroethics Challenge Informed by ...

Target Article Imaging or Imagining? A Neuroethics Challenge Informed by Genetics Judy Illes, Stanford University Eric Racine, Stanford University From a twenty-first century partnership between bioethics and neuroscience, the modern field Keywords of neuroethics is emerging, and technologies enabling functional neuroimaging with unprece- neuroethics dented sensitivity have brought new ethical, social and legal issues to the forefront. Some neuroimaging issues, akin to those surrounding modern genetics, raise critical questions regarding predic- neuroscience tion of disease, privacy and identity. However, with new and still-evolving insights into our and ethics neurobiology and previously unquantifiable features of profoundly personal behaviors such bioethics as social attitude, value and moral agency, the difficulty of carefully and properly interpreting genetics the relationship between brain findings and our own self-concept is unprecedented. Therefore, while the ethics of genetics provides a legitimate starting point—even a backbone—for tackling Open Peer ethical issues in neuroimaging, they do not suffice. Drawing on recent neuroimaging findings Commentaries and their plausible real-world applications, we argue that interpretation of neuroimaging data Donald Kennedy, p. 19 is a key epistemological and ethical challenge. This challenge is two-fold. First, at the scientific Benjamin S. Wilfond level, the sheer complexity of neuroscience research poses challenges for integration of knowl- and Vardit Ravitsky, p. 20 edge and meaningful interpretation of data. Second, at the social and cultural level, we find that Lynette Reid interpretations of imaging studies are bound by cultural and anthropological frameworks. In and Francoise Baylis, p. 21 ¸ particular, the introduction of concepts of self and personhood in neuroimaging illustrates the Paul J. Ford interaction of interpretation levels and is a major reason why ethical reflection on genetics will and Cynthia S. Kubu, p. 23 only partially help settle neuroethical issues. Indeed, ethical interpretation of such findings will Raymond De Vries, p. 25 necessitate not only traditional bioethical input but also a wider perspective on the construction Jocelyn Downie of scientific knowledge. and Michael Hadskis, p. 27 Hubert Doucet, p. 29 Kathinka Evers, p. 31 INTRODUCTION roethics has emerged. While neuroethical discus- Bartha Maria Knoppers, p. 33 sion and debate about psychological states and phys- Chris Buford What a sensation stethoscopy caused! Soon we will iological processes date back to the ancient philoso- and Fritz Allhoff, p. 34 have reached the point where every barber uses it; phers, advanced capabilities for understanding and Ari Schick, p. 36 when he is shaving you, he will ask: ’Would you monitoring human thought and behavior enabled care to be stethoscoped, sir?’ Then someone else will by modern neurotechnologies have brought new invent an instrument for listening to the pulses of the ethical, social and legal issues to the forefront. They brain. That will make a tremendous stir, until in fifty draw on and extend anatomo-clinical approaches to years’ time every barber can do it. Then, when one has had a haircut and shave and been stethoscoped cerebral localization and functional specialization (for by now it will be quite common), the barber will that began in the 16th and 17th centuries, after a ask, ’Perhaps, sir, you would like me to listen to your hiatus of more than two millennia from the days brain-pulses?’ of Aristotle and Hippocrates (300 and 400 BCE; —Kierkegaard, 1846 Marshall and Fink 2003). Some issues, akin to those surrounding modern genetics, raise critical From a twenty-first century partnership be- questions regarding prediction of disease, privacy tween bioethics and neuroscience, modern neu- and identity. However, with new and still-evolving The American Journal of Bioethics, 5(2): 5–18, 2005 ajob 5 Copyright c Taylor & Francis, Inc. ISSN: 1526-5161 print / 1536-0075 online DOI: 10.1080/15265160590923358

The American Journal of Bioethics insights to our neurobiology and previously un- neuroimaging illustrates the interaction of interpre- quantifiable features of profoundly personal behav- tation levels. Addressing the challenge will involve iors such as social attitude, value and moral agency, creative human imagination and conscious aware- the difficulty of carefully and properly interpret- ness of scientific and cultural presuppositions. ing the relationship between brain findings and our This paper, therefore, explores the evolution of own self-concept is unprecedented. Ways of tack- functional brain imaging capabilities that have led ling practical questions in neuroimaging will de- to bold new findings and claims about behavior in pend on how we deal with the fundamental one health and disease. We draw on recent neuroimag- of interpretation—the principal reason that tradi- ing research and their proposed applications. Taking tional bioethics analysis, as laid out in the ethics of a closer look at how genetics has been analyzed from genetics, will not suffice as a guide. an ethical standpoint, we compare issues raised in Consider, for example, the following sampling genetics with issues in functional neuroimaging us- of article titles appearing in the scientific literature ing functional magnetic resonance imaging (fMRI) the past two to three years: “The Good, the Bad as our model. Finally, we discuss interpretation of and the Anterior Cingulate” (Miller 2002), “Morals neuroimaging data as a key epistemological and eth- and the Human Brain: A Working Model” (Moll ical challenge, inescapable for neuroethics and in- et al. 2003), “Strategizing in the Brain” (Camerer tertwined with the history of neuroscience. 2003), “The Medial Frontal Cortex and the Rapid Processing of Monetary Gains and Losses” (Gehring FUNCTIONAL NEUROIMAGING and Willoughby 2002) or “The Neural Basis of Eco- From generations of work by neurotechnologically nomic Decision-Making in the Ultimatum Game” curious and skilled scientists and engineers, pow- (Sanfey et al. 2003), as well as those appearing in erful functional neuroimaging tools have been in- popular print media, such as “How the Mind Reads troduced to the modern era. The most prominent Other Minds” (Zimmer 2003), “Tapping the Mind” tools to date, electroencephalography (EEG), mag- (Wickelgren 2003), “Why We’re So Nice: We’re netoencephalography (MEG), positron emission to- Wired to Cooperate” (Angier 2002), and “There’s mography (PET), single photon emission computed a Sucker Born in Every Medial Prefrontal Cortex” tomography (SPECT) and functional Magnetic Res- (Thompson 2003). From these, we observe that onance Imaging (fMRI), have provided a continuing quantitative profiles of brain function—“thought stream of information about human behavior. maps”—once restricted to the domain of medical re- One of the oldest approaches dates back to 1929, search and clinical neuropsychiatry, may now have when neuropsychiatrist Hans Berger announced the a natural relevance in our approach to daily life. invention of the electroencephalogram and showed This trend conceivably introduces possibilities— that the relative signal strength and position of elec- or at least desires—for using brain maps to assess trical activity generated at the level of the cere- the truthfulness of statements and memory in law, bral cortex could be measured using placement of profiling prospective employees for professional and electrodes at the scalp (Karbowski 1990). With its interpersonal skills, evaluating students for learn- exquisite temporal resolution, the stimulus evoked ing potential in the classroom, selecting investment EEG response “event related potential” (ERP) was managers to handle our financial portfolios, and the first tool to unveil fundamental knowledge even choosing lifetime partners based on compati- about the working of the human brain in near ble brain profiles for personality, interests and de- real time. Over time, other imaging modalities sires. Further, these trends bring to the foreground have come to achieve this goal by capitalizing on what would appear to be a strict epistemological brain signals such as extracranial electromagnetic challenge at the core of neuroethics—proper inter- activity (MEG), metabolic activity and blood flow pretation of neuroimaging data. The challenge will (PET and SPECT), and regional blood oxygenation prove to be two-fold. First, at the scientific level, (fMRI) that yield different and complex measure- the sheer complexity of neuroscience research poses ments of functional activity (for a very readable challenges for integration of knowledge and mean- anthropologic perspective on PET specifically, see ingful interpretation of data. Second, at the social Dumit 2004). By and large, all utilize comparison and cultural level, we find that social interpreta- or subtraction methods between two controlled con- tions of imaging studies are bound by cultural and ditions, heavy statistical processing, and computer anthropological frameworks. In particular, the in- intensive data reconstructions to produce the col- troduction of concepts of self and personhood in orful maps with which we have become familiar. 6 ajob March/April 2005, Volume 5, Number 2

Imaging or Imagining? Figure 1. Experimental (“B” state) images are subtracted from control (“A” state) images to achieve regional activation maps with fMRI. (Courtesy of Gary H. Glover, Lucas MRS/MRI Center, Stanford University) All have roots in the diagnosis and intervention of Figure 1. The surplus of oxygenated blood recruited the wide range of psychiatric and neurological dis- to relatively active brain regions produces the effects eases known to us, including head trauma, demen- measured by MR. tia, mood disorders, stroke, cancer, seizures, and the impact of drug abuse, to mention but a few. Applications of Functional Neuroimaging The different techniques each have relative ad- in Clinical Medicine, Cognitive Science and Law vantages and disadvantages; these are summarized Beyond the use of fMRI in mapping of salient corti- briefly in Table 1 to provide reference for this discus- cal areas prior to surgical intervention for epilepsy, sion. Given their technical trade-offs, fMRI stands tumors or arteriovenous malformations, other ac- out as likely to have the greatest enduring im- tive efforts to make the technology relevant in the pact on our society outside the realm of academia clinical setting have focused on Alzheimer’s Disease and medicine. It is the widespread availability of (AD), mental illness in adults and pediatric pathol- MR scanners today and the noninvasiveness of the ogy such as attention deficit hyperactivity disorder imaging approach enabled by MR have set fMRI (ADHD; Illes and Kirschen 2003). Applications of apart from other neuroimaging tools and made it fetal MRI have also shown great promise in provid- a model for neuroethical discussions. The activa- ing better diagnosis of structural central nervous tion maps produced by fMRI reflect indirect ef- system anomalies, and functional studies of fetal fects of neural activity on local blood flow under brain blood flow are not lagging far behind. At the constrained experimental conditions. Like PET and opposite end of the life spectrum, first approaches SPECT paradigms, a typical fMRI experiment uti- using fMRI to determine levels of consciousness in lizes a stimulus designed for acquiring the relative patients in minimally conscious or vegetative states difference in brain activity between an experimen- have also been attempted (e.g. Schiff et al. 2005) tal and a control (baseline) task, as illustrated in (Giacino 2003). March/April 2005, Volume 5, Number 2 ajob 7

8 Table 1. Characteristics and Trade-offs of Major Functional Neuroimaging Technologies Measurement Technology Strengths Limitations Notes EEG Electrical activity measured Electro-encephalogram; 8 to Noninvasive, well-tolerated, low cost, Limited spatial resolution compared Tens of thousands of at scalp. >200 scalp electrodes. sub-second temporal resolution. to other techniques. EEG/ERP findings reported in the literature. MEG Magnetic fields measured at Superconducting quantum Noninvasive, well-tolerated, good Cost, extremely limited market and scalp, computed from interference device temporal resolution. availability. source-localized electric (SQUID); ∼80–150 sensors current data. surrounding the head. PET Regional absorption of Ringed-shaped PET scanner; Highly evolved for staging of cancers, Requires injection or inhalation of radioactive contrast several hundred radiation measuring cognition function and contrast agent such as glucose or agents yielding measures detectors surrounding the evolving to a reimbursable imaging oxygen; lag time of up to 30 of metabolic activity and head. tool for predicting disease involving minutes between stimulation and blood flow. neurocognition such as Alzheimer’s data acquisition, limited Disease. availability (fewer than 100 PET scanners exist in US today) given short half-life of isotopes and few locations with cyclotrons to produce them; cost. SPECT Like PET, another nuclear Multidetector or rotating Documented uses mapping psychiatric Requires injection of contrast agent Currently available in two medicine technique that gamma camera systems. and neurological disease including through intravenous line; cost. states (CA and CO) for relies on regional Data can be reconstructed at head trauma, dementia, atypical or purchase without absorption of radioactive any angle, including the unresponsive mood disorders, strokes, physician referral; contrast to yield axial, coronal and sagittal seizures, the impact of drug abuse on emphasis is on ADHD and measures of metabolic planes, or at the same angle brain function, and atypical or Alzheimer’s Disease activity and blood flow. of imaging obtained with unresponsive aggressive behavior. (approx. out-of-pocket CT or MRI, to facilitate cost: $3,000 per study). image comparisons. fMRI Surplus of oxygenated MRI scanner at 1 Tesla to 7 Noninvasive, study repeatability, no Cost of equipment and physics Rapid proliferation of blood recruited to Tesla and higher; 1.5T most known risks. New applications of MR expertise to run and maintain research studies using regionally activated common because of its wide in imaging diffusion tensor maps systems. fMRI alone or in brain. clinical availability. (DTI)—namely, the microstructural combination with other orientation of white matter fibers—has modalities, growing from recently been shown to have good 15 in 1991 (13 journals) to correlation with IQ, reading ability, 2,224 papers in 2003 (335 personality and other trait measures journals), representing an (Klingberg et al. 2000). average increase of 56% per year. Note: Combined modality systems such as EEG and fMRI are becoming increasingly common. PET and SPECT are forerunners to frontier technology in molecular imaging.

Imaging or Imagining? Over the past ten years of fMRI develop- poor functioning in the prefrontal cortex, a locus of ment and expanding boundaries of cognitive neuro- impulse control (Raine et al. 1994). In some cases, science, the innovation has been applied to gain new PET images have been used to argue that a defen- non-health related knowledge about human moti- dant was biologically predisposed to committing a vation, reasoning, and social attitudes. In a compre- crime and, therefore, should be spared a conviction hensive literature review, we demonstrated a steady or death sentence. In at least one court case (People expansion of fMRI studies, alone or in combina- v. Jones) a homicide conviction was reversed because tion with other imaging modalities, with evident the state failed to provide brain scans.1 social and policy implications, including studies of In a relatively new application of EEG, EEG- lying and deception, human cooperation and com- derived “brain fingerprinting” has been promoted petition, brain differences in violent people, genetic as a tool for determining whether an individual influences, and variability in patterns of brain de- is in possession of certain knowledge of a crime velopment (Illes et al. 2003). In one intriguing but (Farwell and Smith 2001). It is the possession— unpublished study, Beauregard et al. (reviewed in or lack of possession—of the relevant facts about a Curran 2003) used a combination of EEG, fMRI crime that brain fingerprinting attempts to quantify and PET to probe neural underpinnings of religious through measures of brain-wave responses to rele- experience (Curran 2003). They are focusing on the vant words or pictures presented at rapid rates on a phenomenon known as unio mystica, a joyous sense of computer screen. When the brain recognizes signif- union with God reportedly experienced by a group icant information—such as crime scene details—it of cloistered Carmelite nuns in Montreal, Canada. responds with a “memory and encoding related mul- Discussion of the potential meaning and practical tifaceted electroencephalographic response.” Un- uses of such deeply personal neuroprofiles is ripe for like polygraph testing that measures an individual’s bioethical consideration. fear of getting caught in a lie by tracking relevant Outside the arenas of medicine and cognitive physiological markers, brain fingerprinting ostensi- science, the legal arena offers an obvious venue for bly measures brain waves emitted when information attempting to translate neuroimaging into mean- stored in the brain is recognized.2 ingful, real-world use. As Hank Greely (2002, 5) New applications of fMRI that bridge cognitive wrote: science and law also have the potential to change approaches to truth verification and lie detection. Neuroscience may provide answers to some of the Langleben et al. (2001), for example, used fMRI ‘oldest philosophical questions, shedding light, for to study neural patterns associated with deception. example, on existence limits, and meaning of free In their landmark experiment, volunteers were in- will.’ It may also provide new ways to distinguish structed to either truthfully or falsely confirm or truth from lies or real memories from false ones. This ability to predict behavior with the help of neuroscience could have important consequences for the 1. In a 1992 New York murder case, People v. Weinstein, judicial system as well as for society as a whole. Weinstein was accused of strangling his wife to death and throwing her body from a twelfth-floor apartment. We- Greely provides an extensive review of the legal is- instein’s functional PET scans and structural MRI images sues in his chapter “Prediction, Litigation, Privacy, revealed an arachnoid cyst, and the evidence was admit- and Property: Some Possible Legal and Social Im- ted in court for the purpose of establishing an insanity defense. The ruling was made despite evidence that such plications of Advances in Neuroscience.” (Greely pathology has no known link to criminal behavior. The 2004). A few cases suitable to elucidating where PET scan depicted the juxtaposition of a black lesion (the ethical models for brain imaging may intersect with cyst) on the red and green colored areas of ‘normal’ brain or diverge from genetics are explored here. activity, and was considered so profound as to prove to the Looking back to 1985, when a Supreme Court court that Weinstein’s brain was not functioning within normal parameters. The prosecution in this case accepted holding in Ake v. Oklahoma imposed a constitutional a manslaughter plea. requirement for states to provide psychiatric assis- 2. Brain fingerprinting played a significant role in the case tance in a criminal defense when the question of of Terry Harrington, for example, whose murder convic- sanity is raised, criminal defendants began to argue tion was reversed and a new trial ordered after he spent that ‘psychiatric assistance’ should include a com- 22 years in prison (State of Iowa v. Terry Harrington). The case dates back to 1977, when Harrington, who was 17 plete neurological evaluation including scans like years old at the time, was convicted of murdering a re- PET or MRI. PET studies have shown that com- tired police officer. When, in 2000, Harrington under- mitted murderers, for example, as a group, have went fingerprinting, his brain did not emit the expected March/April 2005, Volume 5, Number 2 ajob 9

The American Journal of Bioethics deny having a playing card in their possession. on some major ethical, legal and social (ELSI) vari- When subjects gave truthful answers, the fMRI ables, this section examines the extent to which the showed increased activity in visual and motor cor- ethics of genomics can serve as a model for ethical tex. When they were deliberately deceptive, addi- analysis of neuroimaging. tional activations were measured in areas including the anterior cingulate cortex to which monitoring of Discrimination, Stigma errors and attention has been attributed. Langleben Given the growing recognition that health infor- et al. concluded that “essentially, it took more men- mation is not entirely private, Clayton (2003) and tal energy to lie than to tell the truth” (Evans others (e.g., Rothenberg and Terry 2002) have sug- 2002). These results are consistent with those of gested that the most common fear about genetic in- Moll et al. (2003) and Heilman (1997) that im- formation is its potential use in justifying denial of plicate the temporo-polar cortex, insula, precuneus access to health insurance, employment, education and their connections in an extended neural cir- and even financial loans to people with particular ge- cuit that attributes conscious emotions and feelings, netic characteristics or diagnoses. While these issues especially those with a social context, to percep- may not be the immediate ones for neuroimaging, tions and ideations (see also Aldolphs et al. 1995; as we have seen, little stands in the way for sim- Damasio 1994; LeDoux 2003). In the future, there- ilar concerns about neuroprofiling with functional fore, we may not only be able to discern whether an imaging to arise even as neuroimaging techniques individual is being deceptive, but also whether the continue to mature. While neuroscientists tease out deception was premeditated or not.3 artifacts masquerading as neural effects and develop PATHWAYS FROM GENETICS TO analytic methods that provide more intuitive ways NEUROIMAGING SCIENCE of interpreting the data than possible today, there already exists a healthy regard for the novelty and Ellen Wright Clayton (2003) provides a compre- breadth of information that neuroimaging can de- hensive review of the impact that advancements in liver about human health, behavior and cognitive genetics and molecular biology have had on soci- fitness. How will such technology be used advanta- ety, and she argues for genomics as a complex phe- geously to benefit people and society? Could it be nomenon that presents specific challenges for clini- used harmfully for ill-intentioned purposes? Will cians and patients alike. Neuroscience is no less eth- Canli’s paradigms for imaging personality become ically complex, and neuroscientists, like geneticists adopted for triaging team players or weak decision- and nuclear physicists even before them, are increas- makers in the workplace (Canli and Amin 2002) or, ingly gaining awareness about the potential impli- in this post-Columbine era, at the door of our high cations of their research at the bench, in medicine, schools to triage out students with a predisposition and in the public domain (Mariani 2003).4 Drawing to unruly or violent behavior? Perhaps screening for good humor would be more acceptable (Canli et al. electroencephalographic patterns in response to critical 2002; Mobbs et al. 2003). details of the murder. The results were interpreted to It will be the moral obligation of bioethicists suggest that he was not present at the murder site, a conclusion corroborated by the fact that his brain did emit and neuroscientists alike to think proactively about the requisite patterns in response to details of the event the impact that such effects might have on peo- used as his alibi in the case. When confronted with the ple, from the point of view both of benefits such brain fingerprinting evidence, the original prosecution as self-knowledge (Weir et al. 1994) and personal witness recanted his testimony and admitted that he had choice, as well as risks, especially for children and lied during the original trial, falsely accusing Harrington to avoid being prosecuted himself. adolescents at critical stages in their personal and 3. In another fMRI experiment related to deception and educational development (Savelscu 2001). By what more broadly to lying, Schacter et al. (1998) demon- means will anyone resist coercive uses of such tech- strated the potential to discern false from truthful mem- nology if employment or educational opportunity ory. In an even more recent study, Anderson et al. (2004) are at stake? If the paradigms of Golby et al. (2001), showed areas of neural activation in the dorsolateral prefrontal cortex associated with the active suppression of Phelps et al. (2003), or Richeson et al. (2003) for memory. studying race and social attitudes could be adopted 4. Even in these early stages, some ire about who is conducting what kind of research and with what motivation has already surfaced, especially with respect to wards and not deliver either scholarly or medical benefit research that would seem only to yield financial re- (Gardner 2003). 10 ajob March/April 2005, Volume 5, Number 2

Imaging or Imagining? for determining eligibility to become a police of- Genetic versus Neuro Determinism ficer, a school principal, or even a national leader, Despite its probabilistic nature, genetic informa- would this be a legitimate allocation of public tion tends to be viewed as a definitive form of health funds? Much mischief beyond discrimination and data. Individuals feel a sense of inevitability with stigma may be created by over-interpretation of any regard to their genes, Clayton (2003) argues, as such results (see also Editorial, “Scanning the So- well as a sense of genetic determinism. Such deter- cial Brain,” Nature Neuroscience, November 2003, minism, or genomic essentialism (Mauron 2003), 1239). has become popular in our culture especially in the way that results of behavioral genetics studies are Privacy of Human Thought communicated to the public. We have read reports Functional neuroimaging poses pivotal challenges about genes for violence, homosexuality, alcoholism to thought privacy. Should thought information and even one for language. The essentialist stance have similar privacy status as genetic information? is strengthened by the fact we have a tendency to Probably not less, but perhaps more. No doubt, in- believe that we are our brains. However, longstand- creased information about the neurobiology of how ing studies of developmental brain plasticity and we think, and potentially why we think what we new activation studies of reorganization after in- think, is likely to cause significant ethical dilem- jury have amply demonstrated that any such reduc- mas for clinicians and researchers, especially as mea- tionist view of complex phenotypes is incomplete sured thought patterns may vary as much with the without consideration of intervening external and hemodynamic properties of the relevant vascula- cultural factors (Ward and Frackowiak 2004). Some ture (D’Esposito et al. 2003) as with gender and have argued that the biological sciences, which deal day-to-day variations in mood and attention (Gur with open systems, are improperly fit for universal et al. 1975). Moreover, they are highly subject to and deterministic laws, as are physics and chemistry variability in the culture and values of the people (Mayr 1998). Arguments that make neuroscience interpreting them (Beaulieu 2002; Dumit 2004). deterministic could well be flawed conceptually and Watson (as cited in Mauron 2003, 245) has stated empirically (Racine 2005). However, given the ten- that the human genome is, at least in part, “what dency to oversimplify complex genetic and brain makes us.” The “brainome” (Kennedy 2003), then, data, discussion of meaning and practical use is a touches more upon who we fundamentally “are”— clear imperative. gnarly territory, at best. With a small leap of faith for real-world validity, the way in which these studies are edging toward Prediction of Disease, Public Health biologic measurements of personhood is illustrated, Countless medical examples exist of symptomatic for example, in a now-landmark trolley car study by individuals who, with an inherited genetic defect Greene et al. (2001; see also Greene 2003). In this for a given disorder, must carefully monitor their moral reasoning experiment, subjects were scanned daily activities to ensure their own health and safety while they made decisions about scenarios in which and that of others. But what of the asymptomatic in- they could, for example, choose to save the lives of dividual who learns from a functional neuroimage five people on a runaway trolley car by pulling a of a predisposition to a disease of the central ner- switch to send it on an adjacent track where one vous system that ultimately affects cognitive per- person stands (and who would not survive), or to formance and lifelong independence? What are the push one of the people off the trolley and on to the implications for third parties, as in the case of neu- track, thereby blocking the movement of the trol- rogenetic disorders, for which functional patterns ley and saving the remainder of the group. Other may surface as sensitive predictors of disease? What studies have required research participants to re- is the new role of physicians in the entrepreneurial solve statements of moral content (e.g., “The judge world of self-referred imaging services? condemned the innocent man” or “The elderly are Work on imaging-based diagnosis holds enor- useless”) versus neutral content (“The painter used mous promise for providing new, quantitative evi- his hand as a paintbrush”; Moll et al. 2002). All dence for otherwise qualitative diagnoses based on such studies touch upon human thought processes clinical findings, however it also raises compelling that push the envelope of cognitive neuroscience questions about what cautions are needed as patients into a domain of significant social concern in which yearn for earlier and earlier diagnosis about diseases privacy is a vital ingredient. for which cures or even treatments do not yet exist. March/April 2005, Volume 5, Number 2 ajob 11

The American Journal of Bioethics Will such data provide welcome new information where, when, or how a crime occurred, nor individ- or impose new burdens on families, physicians and ual guilt (Committee to Review the Scientific Evi- allied health care professionals? Who will have ac- dence on the Polygraph 2003), the constant stream cess to this technology? How will physicians and of innovative scientific approaches is aimed at de- patients incorporate these new types of data into riving biologic correlates for behaviors committed their reasoning about treatment, compliance and in the past (Illes, 2005) is unrelenting. As we seek life planning? Access to advanced technologies by to understand responsibility of others through their the privileged only, whether for diagnosis, medi- biology, it is incumbent upon us to contemplate, yet cal intervention or for a competitive neurocognitive again, our own responsibilities in interpreting such edge, will only further upset an already delicate and information, and in protecting access and appropri- hardly acceptable status quo. ate use. Confidentiality and Responsibility Crossroads We are in an era of neuroinformatics in which sharing of genetic, brain, and other data is encouraged. In Table 2 we summarize areas where ELSI in ge- In some cases of large federally sponsored research, netics converge with and diverge from neuroimag- brain data sharing is even required (Koslow and ing. These are the crossroads at which we can begin Hyman 2000). With only partial brain informa- to transition to our thinking about the ethics of tion is now needed to identify research partici- making brain maps from our experience with ge- pants, and new imaging genomics studies (Hariri netics. As the discussion above and this table both and Weinberger 2003) coupling genetic informa- show, similarities are striking and span the domains tion with brain mapping (“genotyped cognition”; of both research and clinical ethics. They include Hammann and Canli 2004), major new uncertain- profound practical benefits, including new knowl- ties exist about the safety and confidentiality of edge about the human condition and knowledge data stored in cyberspace. Other issues concern the that informs self-determination and life planning. protection of human subjects, including confiden- They include negatives, such as the potential for tiality and responsibility related to incidental find- personal and legal discrimination, inequities of ac- ings. What if pathology is discovered unexpect- cess, risks to confidentiality, inaccuracies inherent edly in a shared data set? With whom does the to predictive testing of any nature and associated burden of disclosure and care lie—the primary or anxiety (Michie et al. 2002), and commercial use secondary laboratory? Beyond the laboratory, how (Merz et al. 2002). Pressing issues unique to genet- shall commercial use of freely shared brain imaging ics but not to neuroimaging are not apparent, but data in the for-profit sector be defined? No doubt, the reverse is noteworthy in as much as the wide countless other examples exist in research beyond range of technical and subjective factors, including these few. paradigmatic, physiologic and investigator biases in As we have seen, our concept of legal respon- research play into the interpretation of results and sibility may also be changed by neuroimaging. In the global potential for biologizing human experi- the United Kingdom, cautions about the use of neu- ence that reaches far beyond any previous window roimages such as PET in the courtroom have already on individual traits. been expressed. In 2002, for example, at a debate entitled “Neuroscience and the Law” hosted by the INTERPRETATION AS A KEY NEUROETHICAL Royal Institution of Great Britain, forensic psychia- CHALLENGE trist and criminal barrister Eastman argued that the The idea that the genome is the “secular equiva- neuroimaging science is still too imprecise to make lent of the soul” has been legitimately criticized “an unequivocal connection between brain struc- (Mauron 2001). New to neuroethics will be the need ture and behavior.” “Even if . . . psychopaths have to tackle responsibly—with the inevitable and om- physically different brains from other people, does nipresent working hypothesis (or the “astonishing it mean anything? Does an abnormal brain auto- hypothesis” to quote Crick 1997)—that the mind matically mean abnormal behavior? Does it mean a is the brain. Responsible and careful interpretation loss of control sufficient to impact on legal respon- of data will therefore become a crucial issue as we sibility? Do you abolish free will on the basis of wrestle to untangle what we image from what we an odd brain scan?” Even while neuroimaging can- imagine. Here, genetics as a model is limited and not establish moral culpability (Kulynych 1997) of bioethicists will have the greatest role in bringing 12 ajob March/April 2005, Volume 5, Number 2

Imaging or Imagining? Table 2. Comparison of Ethical, Legal and Social Issues in Genetics and Functional Neuroimaging ELSI variables Gene hunting, Gene testing Functional neuroimaging In practice: Risk of discrimination, stigma, Yes Not at present, but growing concern coercion exists for the evolution of the technology and expanding use. Risk to privacy Yes Yes Distributive justice Yes Yes, once the technology moves into mainstream clinical medicine. Diagnostic uses Yes Emerging Prediction Yes Emerging Commercial use Yes Emerging; some limited availability already exists in the direct-to-consumer marketplace. In research Paradigmatic variables: Results Potentially but not considered a Highly significant given variability in subject to variability in test used significant risk. equipment, hypothesis-testing, stimulus design and approaches to data analysis. Physiologic variables: Results No Highly significant given fluctuations, subject to physiologic and for example, in blood flow, mood, day-to-day variations. and gender-related physiology. Investigator variables: Results No, but standards for testing are not Highly significant, especially when subject to variability of widespread. interpretation of data interacts with interpretation. individual social values and culture. Global issues: Biologization of personal thought. Possibly in mental illness and Highly significant as complex neuro-degenerative disease. thought becomes quantified and visualized on brain maps. critical thinking to the field. Fundamentally, the of standards of practice in the laboratory (in fact, challenge is two-fold as proper ethical interpreta- innovation and creativity still define the state-of- tion is a crucial concern at both the scientific and the-art in neuroimaging today) and the medicole- the social level. gal setting creates another layer of complexity for While fMRI today may surpass other neu- drawing conclusions about behavior, responsibility roimaging techniques in its use for understanding and cognitive well-being (Kulynych 1997; Nelkin human behaviors that may have practical relevance, and Tancredi 1989) that will need to be penetrated we are witnessing a dynamic stream of new applica- with appropriately responsive ethical approaches. tions and new technical possibilities. Like genetic With dynamic images in hand, we may forget the testing, models for minimizing harm that may re- epistemological limits of how the images were pro- sult from false positives and inappropriate attribu- duced, including variability in research designs, sta- tions of cause-and-effect to otherwise correlative re- tistical treatment of the data, and resolution. It is sults are critical. Apart from genetic testing, brain worth recalling that, in the past, various models maps can be readily portrayed as iconic proof of of the brain have been proposed by great minds pathology to people at any level of literacy. Yet, only to be seen later as mere imagination of the as we have seen, the brain image represents unpar- brain’s real functioning. Descartes used pneumatics alleled complexity—from the specialized medical as a paradigm to explain how the “animal spirits” equipment needed to acquire a scan, to the array of were produced by the flow of blood from the heart parameters used to elicit activations and the statisti- to the brain (Changeux 1983). Later on, the emi- cal thresholds set to draw out meaningful patterns, nent anatomist Franz Joseph Gall proposed phrenol- to the expertise required for the objective interpreta- ogy to the courts for establishing facts and choos- tion of the maps themselves. Moreover, an absence ing appropriate sentences for convicted criminals March/April 2005, Volume 5, Number 2 ajob 13

The American Journal of Bioethics (Lanteri-Laura 1996). In the twentieth century, Mo- “Humans are forever prone to make premature and niz’s psychosurgery procedures certainly left behind presumptuous claims of new knowledge. . . . One an “unhappy legacy” (Gostin 1980). may think that brain imagery will reveal myster- Today, some scientists and philosophers urge ies of the human mind. But it may only help us that we adopt the computer metaphor, neural net- gradually comprehend the organic, chemical and works or other models to understand brain function. physiological features of the brain rather than pro- However different and in some sense far apart, these vide the keys to unlock the secrets of human be- examples highlight cautions needed in the interpre- havior and motivation.” Whatever the outcomes of tation of brain findings and their intended applica- imaging turn out to be, they will depend on sci- tions. In an issue of the journal Brain and Cognition entific as well as cultural scrutiny of neuroimaging that represented a pioneering venture into ethical research. issues in neuroimaging (Illes 2002), the commu- In a study where neuroscientists have teamed- nity of authors who contributed to it already then up with Buddhist monks to understand the mind cited cautions of interpretation as a common con- and test for insights gained by meditation (Global cern. These cautions have been reiterated by oth- News Wire 2003), culturally–laden concepts such ers (e.g., Gore et al. 2003), and alone justify the as ‘person,’ and ‘emotions’ are being questioned by increasing attention to frontier neurotechnologies, imaging. Some argue that consciousness and spiri- their capabilities and limitations, and new ethical tuality could be changed by such findings on the approaches for thinking about them (see also Blank, brain. Therefore not only does culture penetrate 1999). neuroimaging; neuroimaging is increasingly pen- When links are made between neuroimaging etrating non-scientific culture. This is why neu- findings and our self-concepts in particular, it is roethics needs to consider not only ethics of neu- even clearer that the ethics of genetics can only roscience but also a neuroscience of ethics (Roskies partially help settle ethical issues. Genetics and 2002) and, we may add, reflection on their scientific genomics have provided fertile ground for many and cultural implications. ethical reflections on human nature, but the rela- Regardless of the functional neuroimaging tech- tionship between the brain and the self is far more nology du jour, we are left with lingering inter- direct than the link between genes and personal pretation and other questions that any new ethical identity (Mauron 2003). The locus for integrating approach for brain imaging will have to address. behavior resides in the brain, even if discrete features Time, scholarly dedication and collaboration across are determined by our genes. Whether neurotech- the vested disciplines will help resolve them. Some nology measures that behavior through imaging, of these questions, which will inevitably raise the or manipulates it through implants of neural tissue bar and challenges of interpretation are: or devices, it will fundamentally alter the dynamic between personal identity, responsibility and free r Revisiting a classic dichotomy in the conduct of will in ways that genetics never has. Indeed, neu- research, is there neuroimaging research that we rotechnologies as a whole are challenging our sense can do (or will be able to do) but ought not to? of personhood and providing new tools to society If we were to accept that the biology of social for judging it (Wolpe 2002). processes studied within the constraints of the Interpretation of neuroimaging studies are not laboratory translates seamlessly to real-world va- only bound by scientific frameworks, but also cul- lidity, should the contents of ours minds even be tural and anthropological ones. Consider concepts studied this way (Foster et al. 2003)? Who should such as “moral emotions” that are based on assump- decide and according to what scientific and cul- tions that some emotions are moral and others not. tural parameters? They illustrate the cultural aspect of the interpre- r What are the trade-offs between cautious research tation challenge, which is based on the fact that the with public oversight versus the potential for self is defined in diverse ways. For example, central over-regulation in a reaction to adverse or reck- to Buddhism is the Doctrine of No-Soul, whereas in less events? Many lessons may be learned from Hinduism, the self is a religious and metaphysical genetics, but “reckless” will surely take on new concept (Morris 1994). Even within Western tra- meaning in discussions about the neurobiology of ditions, that may appear to be monolithic, various moral reasoning and social behavior. beliefs have served as “sources of the self” (Taylor r How can the reductionist approach of neuroimag- 1989). As Winslade and Rockwell (2002) wrote, ing to human behavior be made compatible and 14 ajob March/April 2005, Volume 5, Number 2

Imaging or Imagining? complementary to approaches represented by phi- disease. Recent neuroimaging findings and their losophy, sociology and anthropology? How will proposed applications show that a great number applications based upon this approach interact of new ethical issues will be raised. ELSI variables with wider cultural perspectives on the self? have given us a invaluable starting point, but, neu- r Will the large investment in neuroimaging be roethics will need to address issues of data interpre- justified by new knowledge? Are there some forms tation in great depth both at the scientific and the of funding that should be eschewed because they cultural level. Neuroimaging illustrates this double may lead to methods for thought control or per- challenge remarkably since imaging technologies sonal financial gain? and methodologies are grounded in scientific as- r What new ethical challenges will neurotechnolo- sumptions. Meanwhile, imaging is an area where in- gies bring us in the future? What will the porta- vestigation of social behavior and selfhood is rapidly bility of near infra-red optical imaging offer? Shall increasing and becoming a legitimate endeavor. In- transcranial magnetic stimulation be transferred deed, at the heart of imaging is an effort to make from the medical arena for treating depression sense of an image in need of interpretation. Right to the open market for boosting or fine-tuning along side with the new concept of “imaging neu- cognition like caffeine or other over-the-counter roethics” others like “neuromarketing,” “neuroeco- stimulants? With advances in reporter probes nomics,” “neuroenablement” (Lynch 2004), “neu- (Kim 2003), what ethical approaches will be rotheology” and even “neurocorrection” (Farah et al. needed for managing new information and thera- 2004) have been spawned. All raise concerns about pies brought forward from the coupling of molec- scientifically-warranted and culturally-sensitive in- ular imaging, targeted either in the central ner- terpretation an application. vous system or elsewhere, and gene therapy trials? With the existence of many views about mind and brain, neuroethics will have to foster discussions The answers to these questions will surely not among neuroscientists whose methods may vary and be binary. As in the past, they will depend funda- interpretation of results differ. These discussions mentally on individuals involved and the context will have extend to include meaningful dialogue in which they are confronted. Fresh thinking, espe- with scholars in the humanities about concepts like cially about the relationship between the self and morality, moral judgments and moral emotions— the brain, will have to be elaborated for these new concepts in need of critical appraisal before we can types of brain data as the layers of complexity of seriously investigate their neural correlates. Open interpretation and overall stakes are arguably far dialogue with the public is no less necessary given greater than ever before. Commenting on Aldous that different cultural and religious perspectives Huvley’s Brave New World (1932) written approxi- subject findings to different interpretations and eth- mately 100 years after Soren Kierkegaard’s foresight ical boundaries. Responsible dissemination of infor- on brain pulses, Pontecorvo wrote: mation through the media and public education are also essential in closing the gap between scientists The ethical issues raised by . . . feats of human engi- and concerned citizens, especially as the complexity neering are qualitatively no different from those we shall have to face in the future. The difference will be and abstractness of results increase. quantitative: in scale and rate. Even so, the individ- Interpretation necessitates creative human ual steps may still go on being so small that none of imagination and conscious awareness of scientific them singly will bring those issues forcibly to light: and cultural presuppositions. Hence, the new gen- but the sum total is likely to be tremendous . . . ” (as eration of neuroethicists must be committed to cited in Stevens, 2000; pp. 81–82). openly examining the epistemological limits of imagery (Racine and Illes 2004), interdisciplinary ap- Pontecorvo was partly right: There is no doubt praisal, and public perspectives on these issues. that the sum total is tremendous. He could never Bioethicists will continue to bring ethical knowl- have predicted, however, the extent to which chang- edge to the discussion and identify and clarify moral ing qualities would parallel changing quantities. quandaries; bioethicists however, will also have to work as facilitators of a broader dialogue where ADDRESSING THE CHALLENGE different perspectives can meet and contribute to This paper explored the evolution of functional a deeper understanding of the issues. Therefore, brain imaging capabilities that have led to bold new while in the past technology and ethics may have findings and claims about behavior in health and leapfrogged each other, in this new era, bioethicists March/April 2005, Volume 5, Number 2 ajob 15

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