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Neuroethics: The Ethical, Legal, and Societal Impact of Neuroscience Martha J. Farah Center for Neuroscience & Society, University of Pennsylvania, Philadelphia, Pennsylvania 19104; email: [email protected] Annu. Rev. Psychol. 2012. 63:571–91 The Annual Review of Psychology is online at psych.annualreviews.org This article’s doi: 10.1146/annurev.psych.093008.100438 Copyright c 2012 by Annual Reviews. All rights reserved 0066-4308/12/0110-0571$20.00 Keywords brain imaging, enhancement, free will, privacy, soul Abstract Advances in cognitive, affective, and social neuroscience raise a host of new questions concerning the ways in which neuroscience can and should be used. These advances also challenge our intuitions about the nature of humans as moral and spiritual beings. Neuroethics is the new field that grapples with these issues. The present article sur- veys a number of applications of neuroscience to such diverse arenas as marketing, criminal justice, the military, and worker productivity. The ethical, legal, and societal effects of these applications are discussed. Less practical, but perhaps ultimately more consequential, is the impact of neuroscience on our worldview and our understanding of the human person. 571 Annu. Rev. Psychol. 2012.63:571-591. Downloaded from www.annualreviews.org by University of Pennsylvania on 03/26/12. For personal use only.

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PS63CH22-Farah ARI 31 October 2011 13:38

Neuroethics: The Ethical,Legal, and Societal Impactof NeuroscienceMartha J. FarahCenter for Neuroscience & Society, University of Pennsylvania, Philadelphia,Pennsylvania 19104; email: [email protected]

Annu. Rev. Psychol. 2012. 63:571–91

The Annual Review of Psychology is online atpsych.annualreviews.org

This article’s doi:10.1146/annurev.psych.093008.100438

Copyright c© 2012 by Annual Reviews.All rights reserved

0066-4308/12/0110-0571$20.00

Keywords

brain imaging, enhancement, free will, privacy, soul

Abstract

Advances in cognitive, affective, and social neuroscience raise a hostof new questions concerning the ways in which neuroscience can andshould be used. These advances also challenge our intuitions aboutthe nature of humans as moral and spiritual beings. Neuroethics isthe new field that grapples with these issues. The present article sur-veys a number of applications of neuroscience to such diverse arenas asmarketing, criminal justice, the military, and worker productivity. Theethical, legal, and societal effects of these applications are discussed. Lesspractical, but perhaps ultimately more consequential, is the impact ofneuroscience on our worldview and our understanding of the humanperson.

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Contents

WHY NEUROETHICS,WHY NOW? . . . . . . . . . . . . . . . . . . . . . 572What Can We Do? What Should

We Do? . . . . . . . . . . . . . . . . . . . . . . . . 573What Do We Know? How Should

We View Ourselves? . . . . . . . . . . . . 573NEUROETHICS OF BRAIN

IMAGING . . . . . . . . . . . . . . . . . . . . . . . . 574Ethical Issues, Familiar and New . . . 574Imaging the Mind. . . . . . . . . . . . . . . . . . 574Imaging Individual Minds

and Mental States . . . . . . . . . . . . . . . 575Nonmedical Applications

of Brain Imaging . . . . . . . . . . . . . . . . 576Ethical, Legal, and Societal Issues

in Brain Imaging . . . . . . . . . . . . . . . . 578Brain Privacy . . . . . . . . . . . . . . . . . . . . . . 578Overpersuasiveness

of Brain Images . . . . . . . . . . . . . . . . . 578NEUROETHICS OF BRAIN

ENHANCEMENT . . . . . . . . . . . . . . . 579Ethical Issues, Familiar and New . . . 579Cognitive Enhancement . . . . . . . . . . . . 580Social-Affective Enhancement . . . . . . 580Nonpharmacological

Enhancement . . . . . . . . . . . . . . . . . . . 582Ethical, Legal, and Societal Issues

in Brain Enhancement . . . . . . . . . . 582Voluntary Physician-Assisted

Enhancement . . . . . . . . . . . . . . . . . . . 582Ethical, Legal, and Societal

Implications of CognitiveEnhancement . . . . . . . . . . . . . . . . . . . 583

Ethical, Legal, and SocietalImplications of Social-AffectiveEnhancement . . . . . . . . . . . . . . . . . . . 584

THE NEUROSCIENCEWORLDVIEW . . . . . . . . . . . . . . . . . . . 585Moral Agency and Responsibility . . . 586Religion and the Nature

of Persons . . . . . . . . . . . . . . . . . . . . . . 587Finding Meaning in a

Material World . . . . . . . . . . . . . . . . . 587

WHY NEUROETHICS,WHY NOW?

The word “neuroethics” entered the vocabu-lary of academic neuroscientists and bioethicistsat the beginning of the twenty-first century. Itwas coined by William Safire, a scholar of wordhistory and meaning (for 30 years he wrote theNew York Times column “On Language”) whoalso stayed abreast of developments in neuro-science as chairman of the Dana Foundation.From its first mention in a 2001 Safire col-umn, “neuroethics” has come to refer to a broadrange of ethical, legal, and social issues raisedby progress in neuroscience. To understand theemergence of neuroethics as a field, meriting aname of its own, we must consider some recentscientific history.

For much of the latter twentieth century,genetics was viewed as the science most likely tochallenge our ethical, legal, and social practicesand assumptions (e.g., Silver 1997). Findingsfrom twin studies and other behavioral geneticsmethods demonstrated the substantial role ofgenes in most aspects of human psychology,and the development of molecular geneticspromised to reveal the mechanisms by whichpersonality, intelligence, psychiatric vulnera-bilities, and other traits developed, as well as toopen the door to targeted interventions (e.g.,Parens 2004). By the turn of the century, how-ever, it had become clear that psychologicaltraits bore only the weakest relationships withindividual genes and that the genetics of humanpsychology involve extremely complex patternsof interaction among genes and between genesand environment, limiting the ease with whichtheories could be constructed and also theeffectiveness with which interventions tochange behavior could be achieved (e.g., VanGestel & Van Broeckhoven 2003).

Contemporaneous with the lowering ofexpectations for genetics, neuroscience wasundergoing rapid development into the areasof cognition, emotion, and social processes,thanks in large part to the advent of functionalneuroimaging. Like genetics, neurosciencedeals with the biological essence of persons,

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Figure 1Schematic illustration of the relations between genes, experience, the brain, and behavior.

including their minds and behaviors. However,as represented in Figure 1, neuroscienceencompasses the totality of genetic influenceson behavior combined with environmentalinfluences. Also apparent in Figure 1, thebrain is one causal step closer to behavior thanto genes or features of the environment. Theseconsiderations suggest that neuroscience mayturn out to be far more successful than geneticsin explaining, predicting, and changing humanbehavior. Indeed, so far neuroscience has beenliving up to this promise. For example, whereassingle genes account, typically, for 2% to 4%of the variance in personality traits (Van Gestel& Van Broeckhoven 2003), brain imagingstudies typically capture an order of magnitudemore variance (Farah et al. 2009).

As a result of these developments incognitive, affective, and social neuroscience,neuroscience can now be brought to bear inmany different spheres of human life, beyondthe traditional application area for biologicalscience, medicine. Any endeavor that dependson being able to understand, assess, predict,control, or improve human behavior is, inprinciple, a potential application area for neuro-science. This includes diverse sectors of society,for example, education, business, politics, law,entertainment, and warfare. The goal of thisarticle is to review the current and near-term

role of neuroscience in our lives and evaluateits likely impact on individuals and society.

What Can We Do? What ShouldWe Do?

The next two sections of the article address theissues that emerge from neuroscience-basedtechnologies, in other words, relatively prag-matic issues concerning how the fruits of socialneuroscience can and should be applied. Theseinclude ethical, legal, and social challengesraised by newfound abilities to image the brainand thereby obtain information about mentalstates and personal traits, as well as by ourgrowing ability to intervene in individuals’brain function to alter these states and traits.These first two sections in effect begin withthe question, “What can we do with neuro-science?” and go on to analyze the ethicalquestion that follows, “Should we do it?”

What Do We Know? How Should WeView Ourselves?

The final section addresses neuroethical issuesthat emerge from the impact of social neuro-science on our understanding of human beings.In this section it is the knowledge per se, notits technological applications, that is the focus

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MRI: magneticresonance imaging

Incidental finding:abnormality that isunintentionallydiscovered in theprocess of laboratorytesting

PET: positronemission tomography

of the review. This section includes the ways inwhich our evolving understanding of the hu-man person challenges our long-held beliefsabout morality and spirituality. The questionsof this section are, in effect, “What do we knowabout the neural bases of the human mind?” and“How does this knowledge change the way weview ourselves, as moral and spiritual beings?”

NEUROETHICS OFBRAIN IMAGING

Ethical Issues, Familiar and New

Developments in brain imaging have engen-dered a large literature in neuroethics. Someof this literature is concerned with issues forwhich we can find helpful precedents in clinicalbioethics. For example, now that magneticresonance imaging (MRI) of healthy normalsubjects is a widespread research method, weface the issue of what to do when anatomicalabnormalities or signs of disease are revealedin the course of scanning. Do researchers havea duty to search scans for such abnormalities?If they are not qualified to screen for abnor-malities themselves, must they show them tosomeone who is? Should subjects be allowedto opt out of being informed of such findingsin advance of the scan? There is currently nouniversally accepted procedure for dealing withincidental findings from research scans (Illeset al. 2004). Of course, the ethical issues raisedby incidental findings from brain scans are notfundamentally different from those that wouldbe raised by imaging other organ systems orby genetic testing. Although important workremains to be done on this topic, the issues arenot particularly unique to the brain.

Another important neuroethical issue withclose analogies in clinical bioethics is predic-tive and diagnostic imaging for progressivediseases that lack effective treatments, suchas Alzheimer’s disease (Karlawish 2011). Suchscans are intended for research aimed at under-standing the pathophysiology of neurodegener-ative disease and the development of treatmentsfor use in the presymptomatic phase. However,

these scans could be used for other reasons bythe “worried well” of the baby boomer genera-tion or their worried employers or insurers. Insuch cases, the benefits of foreknowledge, forexample the greater opportunity to plan, mustbe weighed against the psychological burden ofthis knowledge and its potential impact on em-ployability or insurability. As with the problemof incidental findings, the ethical, legal, and so-cietal dimensions of this problem are largelyfamiliar from clinical bioethics outside of brainimaging, particularly in the area of genetictesting.

In other cases, brain imaging raises new eth-ical, legal, and social issues that stem directlyfrom the special relationship between brain andmind. The ability of brain imaging to deliverinformation about our psyches—about who weare and what we might be thinking or feel-ing while in the scanner—opens up a rangeof ethical challenges with few, if any, directprecedents. These relatively new neuroethicalissues provide the focus for the remainder of thissection.

Imaging the Mind

Since Michael Posner and Marcus Raichle firstadapted positron emission tomography (PET)scanning to the study of cognitive processesin the 1980s, brain imaging revolutionized thestudy of psychology and neuroscience and ledeventually to the scientific capabilities that to-day present ethical, legal, and social challengesas well as benefits.

The first phase of this process was theharnessing of functional brain imaging forthe study of human psychology, which re-quired the ability to isolate the brain activityassociated with specific component mentalprocesses from the totality of brain activityevoked by the numerous processes engagedwhen people perform psychological tasks. Todo this, the pattern of brain activity associatedwith performing one task was subtracted fromthe pattern of brain activity associated with an-other task, hypothesized to require all the samecomponent processes as the first along with one

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additional process (see, e.g., Posner & Raichle1994). By the assumptions of the subtractionmethod, the difference image resulting fromthe subtraction of two images would depictthe brain activity associated with that singleadditional process. The subtraction methodand later elaborations and variations, such asconjunction and disjunction and parametricand habituation methods, allowed imagingto isolate individual psychological processes.Instead of presenting us with the superpositionof all processes involved in performing a task,for example solving mental rotation problems,these methods enabled researchers to disen-tangle the component processes, for exampleperceiving the 3-D form of the mental rotationstimulus, the process of mentally rotating thatstimulus, and the process of responding. Theseadvances enabled the rapid growth of cognitiveneuroscience in the 1990s.

Although the methods just described wereinitially applied to the study of cognition(e.g., language, memory, visual perception),by the mid-1990s researchers had begun touse them for the study of emotion (see, e.g.,Phan et al. 2002 for a review of early work inthis area). Soon thereafter the field of socialneuroscience was born, and the more complexemotions and cognitions involved in interper-sonal processes became subjects of study infunctional neuroimaging (see, e.g., Lieberman2007 for a review). During the same period,functional neuroimaging methods developedfurther to include better statistical solutionsto the false-positive activations in whole-brainanalyses and methods for studying functionalconnectivity (Aguirre 2010), both of whichhelped to realize the potential of functionalimaging to illuminate the functioning of thebrain as a whole system, and were joined bynew methods for studying structure, includingvoxel-based morphometry and diffusion tensorimaging (Le Bihan 2001, Mechelli et al. 2005).

As a result of continued methodologicaldevelopment of imaging, and especially itsgrowing use for the study of affective and socialprocesses, by the turn of the century neu-roimaging had entered the public’s awareness.

Voxel-basedmorphometry: MRImethod of assessingthe size and shape of abrain by comparing it,voxel by voxel, toreference brain

Diffusion tensorimaging: MRImethod using degreeof anisotropy of waterdiffusion to assess theintegrity of whitematter tracts in thebrain

Pictures showing the brain bases of deeplypersonal aspects of ourselves—fear, joy, love—made striking news. Brain imaging seemedto show that our highest human virtues andworst human vices were localizable functionsof the brain, revealed as colored hot spots onanatomically detailed grayscale images. Eventhe scientifically sophisticated among us hadto admit to the occasional feeling of wonderor awe when viewing such evidence. As isdiscussed in the final section of this review,by demonstrating the existence of physicalcorrelates of our most important humanqualities and experiences, neuroimaging hascontributed to a fundamental change in howwe think of ourselves and our fellow persons.

Imaging Individual Mindsand Mental States

One more type of methodological develop-ment was needed in order for brain imaging tobecome a tool that poses practical ethical, legal,and social challenges. This was the develop-ment of methods for disaggregating imagingdata by subject and by mental event. In the earlydecades of functional brain imaging research,inferences were made about groups of subjectswith the goal of generalizing about typicalnormal brains or about brains that are typicalof a group of interest (e.g., males or females,depressed or nondepressed people). For suchanalyses, variation between subjects within thegroup was treated as a form of measurementerror. Similarly, imaging experiments generallyinvolved a small number of conditions, forexample a baseline condition and one or twoexperimental conditions, with many trials percondition. The trials were treated as repeatedmeasures of the condition of interest and notanalyzed for the sake of making inferencesabout the individual events themselves. Thischanged around the turn of the century, withdifferent groups of researchers focusing on theproblem of analyzing the results of single trialsand on the study of individual differences inbrain activity.

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Implicit AssociationTest: a reaction-timetest developed in socialpsychology to assessthe degree to whichdifferent concepts areassociated insomeone’s mind

fMRI: functional MRI

If cognitive neuroimaging was the achieve-ment of the 1980s and social-affective neu-roimaging was the achievement of the 1990s,then the imaging of individual people and indi-vidual mental states was the achievements of thenext decade, the 2000s. This enabled imaging todeliver information with pragmatic ethical, le-gal, and societal implications, such as correlatesof the social and affective traits of individuals.Examples of research on individual differencesinclude many examples with the potential to bedeveloped as tools for screening or assessment.Such uses could benefit individuals and societyor introduce new harms. Consider the follow-ing findings, all of which are the results of basicresearch, not attempts at measurement.

Personality traits such as neuroticism,extraversion, conscientiousness, and empathy,which have been the mainstays of self-reportstudies of individual differences in personality,have become active topics of brain imagingresearch (Hamann & Canli 2004). In addition,many traits that fall outside the realm of tradi-tional personality psychology, such as attitudesand propensity to violence, have also beenfound to have neural correlates measurableby brain imaging. For example, an early andinfluential study by Phelps and collaboratorsfound that white subjects’ amygdala activationcorrelates with the degree of unconsciousnegative evaluation of black faces (Phelps et al.2000). Specifically, the discrepancy betweenamygdala activation to black and white facescorrelated with the magnitude of unconsciousbias against blacks measured in the ImplicitAssociation Test (Greenwald et al. 1998).Coccaro et al. (2007) showed subjects with andwithout a history of impulsive aggression pho-tos of faces displaying different emotions whilemeasuring neural responses to these photoswith functional MRI (fMRI). In addition tofinding overall differences between aggressiveand nonaggressive subjects in their responseto the sight of an angry face, including greateractivation of the amygdala and less activation ofthe presumably regulatory orbitofrontal cortex,they also found a correlation between amygdala

activation and aggression. The more aggressiveone’s behavior, measured over one’s lifetime,the higher the activation of the left amygdalato angry faces. Turning to a more desirabletrait, altruistic cooperation, Rilling et al. (2002)scanned subjects while they played an iteratedPrisoner’s Dilemma game and assessed therelationship between the tendency to prolongmutually cooperative play and the activation ofreward-related brain areas by such cooperation.They found a correlation between cooperativebehavior in the scanner and the activationit evoked in the ventral striatum, an areaassociated with the enjoyment of rewards frommoney to chocolate (Delgado 2007). In thesestudies just cited the correlations are moderatein size, between 0.5 and 0.7, and this accordswell with the majority of appropriately ana-lyzed fMRI studies of individual differences insocial and affective traits (e.g., Vul et al. 2009).

Nonmedical Applicationsof Brain Imaging

Given the moderately strong relationships thatexist between some psychological traits andimaging measures, could imaging be used asa method for assessing personality or ability?My colleagues and I addressed this issue insecondary analyses of data published prior to2007, taking into account both the predictionerror attributable to the less-than-perfect cor-relations and the prediction error attributableto the less-than-perfect estimates of the cor-relations themselves (Farah et al. 2009). Weconcluded that by scanning a new subject in atypical imaging paradigm from this literature,one could gain a modest degree of informationabout an individual. For example, if the bestprediction from a person’s brain activity is to avery high or low value of a psychological trait,one could conclude that the person is in factunlikely to be low or high, respectively, on thattrait. Such minimal predictive power would notbe a practical use. However, among the stud-ies we reviewed, some were more predictive.Assuming that imaging protocols with different

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tasks and different regions of interest pro-vide nonredundant information about traits,more precise prediction may be possible bycombining paradigms for the purpose of traitmeasurement.

Whereas brain imaging is not being usedto assess psychological traits for practicalpurposes, it is being used to assess psycho-logical states. One state that researchers haveattempted to read from brain activation islying. Early studies of deception were aimedat the basic science goal of characterizingthe differences in brain activation betweenlying and truth-telling (e.g., Langleben et al.2002) and showed that the anterior cingulatecortex as well as regions of prefrontal andparietal cortex were more active during lies (forreviews, see Bles & Haynes 2008, Christ et al.2009). Some of the more recent research ondeception with fMRI has been aimed explicitlyat the reverse inference of determining thetruthfulness of individual statements on thebasis of brain activation. Two companiescurrently offer fMRI lie detection services:Cephos (http://www.cephoscorp.com/) andNo Lie MRI (http://www.noliemri.com/).Among the purposes for which they advertisetheir services are vindication “if your word,reputation or freedom is in dispute,” reductionof “risk in dating,” and as a substitute fordrug screening, resume validation and securitybackground checks in employment screening.Both companies have scanned defendants inlegal cases, but as of this writing neither hassucceeded in having its results admitted as evi-dence in court. In the 2010 case of United Statesv. Semrau, the Cephos method was the subjectof a hearing to determine whether it met thecriteria for admissibility set out in Daubertv. Merrell Dow Pharmaceuticals. The courtdetermined that it did not satisfy the Daubertrequirements because its accuracy outside of ar-tificial laboratory tasks had not been examined.In this connection it is worth noting that anelectroencephalography (EEG)-based methodfor detecting deception has been used forseveral years in Indian courts (Aggarwal 2009).

Reverse inference:inferring apsychological statefrom brain data ratherthan starting with aknown psychologicalstate and discoveringits neural correlate

EEG: electroen-cephalography

Neuromarketing is another example ofthe use of brain imaging to assess mentalstates for a practical purpose. The emotionsand motivations of consumers are crucial formany marketing decisions, from brand identityto pricing, but consumers are notoriouslypoor at reporting these aspects of their ownpsychology. The prospect of directly “reading”consumers’ brain states is therefore of great in-terest to marketers. In addition, brain imagingis relatively well suited to this type of reverseinference. Compared with some psychologicalstates, states of liking and wanting have arelatively straightforward relation to patternsof brain activity. EEG and fMRI have thereforebecome widely used tools in market research.

Published research in the field of neu-romarketing has illuminated the ways inwhich packaging design, price, brand identity,spokesperson celebrity, and other marketingfactors that are separate from the productitself affect neural responses to the productand how accurately those neural responsespredict purchasing decisions (for reviews, seeHubert & Kenning 2008, Lee et al. 2007). Thesuccess of neuromarketing as a business toolis harder to assess, but the list of companiespaying for neuromarketing suggests that manycorporate decision makers have faith in it.Forbes magazine reported that this list includesChevron, Disney, eBay, Google, Hyundai,Microsoft, Pepsico, and Yahoo (Burkitt 2009).

The techniques of neuromarketing are notlimited to selling products and services. Theyhave also been used to study preferences forhealth behaviors (Langleben et al. 2009) andpolitical candidates (Westen et al. 2006). Thefirm FKF Applied Research published advice,based on their fMRI studies, to American pres-idential candidates for the 2008 election in theOp Ed pages of the New York Times (Iacoboni2007). Their advice received widespread at-tention in the media and online (Aron et al.2007, Farah 2007; see also Iacoboni 2008,Poldrack 2008). Less public attempts to under-stand voters’ reactions to candidates on the basisof measures of brain function have reportedly

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been carried out at the request of specific polit-ical campaigns (Lindstrom 2008).

Ethical, Legal, and Societal Issuesin Brain Imaging

Concerns about the ethics of brain imaging fallinto two general categories, which can roughlybe described as the “damned if you do anddamned if you don’t” categories. To the extentthat brain imaging can actually deliver usefulinformation about a person’s mental states ortraits, the issue of privacy is important. To theextent that it cannot, but people believe thatit can, the issue of public misunderstanding isimportant.

Brain Privacy

A number of writers have commented on thepotential threat to privacy posed by functionalneuroimaging (e.g., Comm. Sci. Law, Assoc.Bar City N.Y. 2005; Hyman 2004). On theface of things, brain imaging poses a novelchallenge to privacy in that it can in principledeliver information about thoughts, attitudes,beliefs, and traits even when someone offers nobehavioral responses.

More concretely, and perhaps more impor-tantly, imaging-based psychological investiga-tions lend themselves to stealth uses in ways thatmore conventional paper-and-pencil or otherlow-tech methods do not. Both structural andfunctional brain images can be obtained withconsent for one purpose but later analyzed forother purposes. Furthermore, in many studiesthe stimuli and instructions do not reveal thenature of the psychological information beingsought. For example, in two of the studiescited previously, unconscious racial attitudesand impulsive aggression were both correlatedwith brain activity evoked by simply viewingpictures of faces (Coccaro et al. 2007, Phelpset al. 2000). Hence, in principle it seems possi-ble to obtain information about racial attitudesand aggressive tendencies without subjects’knowledge or consent by misleading them intothinking the study concerns face perception.

Overpersuasiveness of Brain Images

At present, the problem of public misunder-standing of neuroimaging is a more immediatechallenge than is the problem of mental pri-vacy. A number of authors have suggested thatlaypersons may attribute greater objectivityand certainty to brain images than to othertypes of information about the human mind(Dumit 2004, McCabe & Castel 2007, Racineet al. 2005, Roskies 2008). This may contributeto the premature commercialization of brainimaging for various real-world applications.

Tovino (2007) outlines a range of pos-sible regulatory responses to nonmedicalneuroimaging, aimed primarily at protectingconsumers and citizens from overhyped andunderperforming methods. She is rightlycautious about strict or blanket restrictions.Not all premature or unvalidated applicationsof neuroimaging pose serious danger, andentrepreneurs should have some motivation todevelop new solutions to societal problems us-ing brain imaging. Different application areascall for different levels of regulatory protection.For example, lie detection for vetting potentialdates (an advertised application) should nothave to meet the same standards of evidenceas for national security-related interrogations.It has even been argued that brain-based liedetection need not meet the same standardsof accuracy expected of scientific evidenceto be appropriate legal evidence (Schauer2010).

From a global perspective, it seems unlikelythat regulation of neuroimaging applicationswill be uniform. Thus, efforts to discourageimaging-based approaches to problems withpotentially significant economic or security rel-evance have an element of unilateral disarma-ment. Although the risks of premature adoptionof these methods, to individuals and society, aresubstantial, overly restrictive policies can alsobe counterproductive. Neither the unrealisticscience fiction scenarios of mind reading northe irresponsible hawking of unvalidated meth-ods are reasons to discourage the developmentand validation of neuroimaging approaches to

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lie detection, employment or security screen-ing, business, and education.

NEUROETHICS OF BRAINENHANCEMENT

Ethical Issues, Familiar and New

As used in the neuroethics literature, “brain en-hancement” refers to interventions that makenormal, healthy brains better, in contrastwith treatments for unhealthy or dysfunctionalbrains. People have been chemically enhancingtheir brains for millennia, far longer than theyhave been treating brain disorders. Coffee, tea,coca leaves, and alcohol are among the familiarsubstances used to alter brain chemistry for im-proved cognition or mood. Yet with the adventof biological psychiatry, drugs developed forthe purpose of treating neuropsychiatric diseasecan now be used by healthy people for enhance-ment, greatly increasing the variety and potencyof methods for adjusting our brain states chem-ically. In addition, nonpharmacologic means ofaltering brain function, for example by mag-netically stimulating specific brain regions toachieve specific psychological effects, are nowpoised to make the same transition from clini-cal to lifestyle use. These developments raise ahost of new questions concerning personal im-provement in the age of psychopharmaceuticalsand neurotechnology.

One important set of issues concernsthe tangled relationships connecting thepharmaceutical industry, university research,regulatory oversight, and physician education,especially in the United States (Lo & Field2009). These problems are not unique topsychopharmacology, although they weighespecially heavily there for at least two reasons.One is the chronic nature of many neuropsy-chiatric conditions. Drugs that must be takenfor decades by each individual patient aresubject to especially powerful profit motives.Another is the problematic state of psychiatricnosology and the associated shortcomings ofcurrent diagnostic criteria. In the absence ofvalid diagnostic tests, it is difficult to draw the

line between sick and borderline or borderlineand well. Treatment of milder cases, like treat-ment for longer periods, increases sales. Thusthe corporate profit motive plays a role in theexpanding use of psychopharmacology by therelatively healthy. However, this can be viewedas a special case of a more general trend towarddeveloping and marketing of medications forchronic conditions and for treating less severeforms of those conditions, a trend that is alsoevident in medical approaches to high bloodpressure, high cholesterol, and diabetes.

The safety of brain enhancement is anothertopic of relevance to neuroethics. Most peoplefind it reasonable to hold enhancements to ahigher standard of safety than treatments. Interms of risk:benefit ratio, this is because we as-sume that treatments have greater benefits thanenhancements; the value of returning someoneto health is greater than the value of makinga healthy person even better off. Yet little isknown about the long-term safety of usingneuropsychiatric medications or neurotechnol-ogy for enhancement. Indeed, relatively littleis known about the long-term effects, both effi-cacy and safety, of many neuropsychiatric treat-ments, and evidence concerning their effects onnormal healthy subjects is generally confinedto early, short-term clinical trials (Hackshaw2009). The safety of enhancement has recentlyattracted attention in the neuroethics litera-ture, and deservedly so. Of particular concernhave been the risks associated with prescriptionstimulants, including heart attack, psychosis,and addiction (Chatterjee 2009, Volkow &Swanson 2008). Of course, the question ofhow to weigh safety against potential benefitsand methods for assessing safety are essentiallythe same, whether one is considering cognitiveenhancement or cosmetic surgery.

In the remainder of this section we explorethe more distinctive neuroethical issues asso-ciated with the enhancement of cognitive andsocial-affective brain functions. By manipulat-ing our intellects, personalities, and moods, arewe distorting our own nature? Or are we ex-pressing that very nature, as a species driven toinnovate and improve our world and ourselves?

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ADHD: attentiondeficit hyperactivitydisorder

SSRI: selectiveserotonin reuptakeinhibitor

Cosmetic psy-chopharmacology:the use of psychiatricmedications toenhance mood orpersonality

How will the growing trend toward brain en-hancement affect us, as individuals and as asociety?

Cognitive Enhancement

Amphetamine has a long history of nonmedicaluse (Rasmussen 2008), and the past decadesaw a distinct rise in its use as a study aidon college campuses in the form of Adderall,a mixture of amphetamine salts intendedprimarily for the treatment of attention deficithyperactivity disorder (ADHD). The cognitiveneuroscience literature is mixed concerningthe effectiveness of stimulants as cognitiveenhancers for normal healthy subjects, withsome studies finding improvements in learningand executive function and some finding nullresults or even occasionally impairment forsubsets of subjects (Smith & Farah 2011).Nevertheless, many college students are atleast occasional users. The results of a 2001survey of more than 10,000 American collegeand university students showed that 7% hadused a prescription stimulant such as Adderallnonmedically, and this figure ranged as high as20% on some campuses (McCabe et al. 2005).Smaller and less scientific samples have pro-duced estimates as high as 50% in more recentyears (DeSantis et al. 2009). A number of stud-ies reviewed by Smith & Farah (2011) indicatethat academic performance enhancement wasthe most common reason students use thesedrugs, although other “lifestyle” uses such asweight control were occasionally reported.

Anecdotal evidence and informal journalists’surveys suggest that some professionals, as wellas students, have added amphetamine and otherstimulants to their work routines (Arrington2008, Madrigal 2008, Maher 2008, Sahakian &Morein-Zamir 2007, Talbot 2009). Among thenewer compounds mentioned in such surveysis modafinil. This drug was initially developedto reduce sleepiness in narcoleptic patients,but it also counteracts many of the cognitivesymptoms of sleep deprivation in healthynormal users, allowing for more comfortableand productive “all-nighters” (Arrington 2008,

Hart-Davis 2005, Madrigal 2008, Plotz 2003).Some research suggests that modafinil mayalso enhance aspects of cognition in healthypeople who are not sleep deprived (Turneret al. 2003). The ability to control when onegets sleepy, and perhaps even work smarter aswell as work longer, has obvious allure.

Looking to the next decade or two, a num-ber of new cognitive enhancers are likely tobe available. Several companies are developingdrugs to manipulate learning and memory.Spearheaded by scientists such as Eric Kandel,Mark Bear, Gary Lynch, Tim Tully, and othermolecular neurobiologists, these companies aredeveloping drugs designed to treat cognitivedisorders and also to enhance the memoryabilities of normal people (Marshall 2004). Ifone projects the market for normal memory-enhancing drugs from sales of nutritionalsupplements sold for this purpose, it is clearthat the economic motivation is huge to de-velop memory-enhancing drugs to help normalpeople deal with their complex lives. Drugs tosuppress unwanted memories are also the objectof research and development (Singer 2009).

Social-Affective Enhancement

Neuroscientists have succeeded in manip-ulating normal levels of mood, personality,empathy, trust, aggression, and so forth,although little of this work has been translatedinto clinical or enhancement use. The modernage of social-affective enhancement began withthe introduction of selective serotonin reup-take inhibitors (SSRIs) such as Prozac in the1980s. These drugs offered much-needed newtreatment options for patients suffering fromdepression and anxiety disorders and had widersocietal effects as well. Peter Kramer (1997)foretold many of the current dilemmas con-cerning the manipulation of mood, personality,and identity in his book Listening to Prozac, coin-ing the term “cosmetic psychopharmacology.”

Any discussion of brain enhancement mustaddress the question of where to draw theline between enhancement and treatment. Forcognitive enhancement, the question is usually

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framed in terms of diagnostic boundaries be-tween everyday distractibility and ADHD, orbetween normal cognitive aging and demen-tia. In the case of SSRIs for social-emotionalenhancement, the question is more complex,partly because there are so many different ther-apeutic uses of SSRIs—including depression,premenstrual dysphoria, general anxiety, so-cial anxiety, obsessive-compulsive disorder—and partly because the relevant diagnosticboundaries appear to have shifted because ofthe SSRIs themselves. In the case of depres-sion, antidepressant medications before Prozachad more troublesome side effects and weretherefore reserved for patients with major de-pression. The greater tolerability of SSRIs,combined with the pharmaceutical industry’senergetic marketing to patients and doctors, hasled to a larger number of less-ill patients usingthese drugs and to a revision of diagnostic cat-egories (Healy 2004). As the division betweenpathology and health moves to include morepeople on the pathological side of the line, usesof medication that would originally have beenconsidered enhancement become therapy.

Antidepressants are now the most widelyused class of drugs in the United States, withan estimated 10% of the population havingreceived a prescription for them in the year2005 (Olfson & Marcus 2009). In light of this,recent findings that SSRIs alter personality takeon broad societal significance. A recent study indepressed patients found that the SSRI parox-etine affects personality above and beyond itseffect on depression (Tang 2009). The mostpronounced effect on personality was on thetrait of neuroticism, the tendency to experiencenegative emotions. Studies that have examinedthe effects of SSRIs in nondepressed subjectshave found that their main effect appears tobe the diminution of negative affect or neu-roticism (Knutson et al. 1998). For example,Knutson and colleagues (1998) administeredparoxetine or placebo for four weeks andassessed the effects of the drug on personalityand social behavior. The drug reduced nega-tive affect, particularly hostility, and increasedaffiliative behaviors. For example, subjects on

the drug spoke fewer commands and insteadmade more suggestions to their partners in aproblem-solving exercise. Among the subjectswho received the drug, plasma levels correlatedwith changes in negative affect and socialbehavior.

In subjects selected for criminal behav-ior rather than psychiatric diagnosis or lackthereof, SSRIs have demonstrated potential foranother socially relevant use: promotion ofprosocial and law-abiding behavior. Impulsiveviolence is associated with abnormalities in ser-atonergic systems, and SSRIs reliably decreaseaggression in individuals prone to violence(Berman et al. 2009, Walsh & Dinan 2001).SSRIs have been found to decrease repeat of-fending in sex offenders and are used for thispurpose, along with hormonal treatments to de-crease sex drive (Bourget & Bradford 2008).

Love, romance, and sexuality in healthynormal people constitute another realm forbrain enhancements. Drugs that affect theseaspects of life through central nervous systemmechanisms have not achieved the successof, for example, Viagra, but more limitedsuccesses have been reported. The drug knownas ecstasy (MDMA) increases feelings ofcloseness and interpersonal connection andcan be used to enhance relationships, althoughserious risks accompany its use (Sessa 2007).Hormone supplementation has been used bylow-testosterone men and postmenopausalwomen to increase libido. A number of newdrugs are being explored for improving sexualfunction in young women suffering from lowlibido (Fitzhenry & Sandberg 2005).

In recent years a wealth of new findings hasemerged on the role of the hormones oxytocinand vasopressin in trust, altruism, and bonding(Donaldson & Young 2008). Intravenous orinhaled doses of these hormones have beenshown to alter the same range of behaviors.Oxytocin has been shown to engender moretrusting and generous strategies in economicgames (Kosfeld et al. 2005, Zak et al. 2007) andto interfere with normal responses to betrayalin such games (Baumgartner et al. 2008). Thisresearch has obvious potential for translation

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TMS: transcranialmagnetic stimulation

tDCS: transcranialdirect currentstimulation

rTMS: repetitiveTMS

into a number of applied domains. It provides aproof of concept for altering the interpersonalrelationships between spouses, parents andchildren, and business associates. It could alsobe used in diplomatic, forensic, and securitycontexts. The practical difficulties of admin-istering oxytocin are being overcome by thedevelopment of oral drugs that target oxytocinreceptors in the brain (Ring et al. 2010).

Nonpharmacological Enhancement

A very different set of technologies influencesbrain function with electronics. The two leastinvasive, and thus most promising for brainenhancement, are transcranial magnetic stim-ulation (TMS) and transcranial direct currentstimulation (tDCS). The physics of these meth-ods is simple, although their physiological ef-fects are another matter. Both methods havetransient and more lasting effects, and the latterhave been found to include enhanced psycho-logical functions in normal volunteers.

With TMS, a magnetic field penetrates thehead and induces current flow that, among itsphysiological effects, triggers action potentialsin targeted neurons. Repetitive TMS (rTMS)involves pulsing the magnetic field, whichcan increase or decrease cortical excitability,depending on the frequency of stimulation.In contrast, tDCS puts the head in a simplecircuit by applying two electrodes, anode andcathodes, to the outside of the head with a weakpower source between them. The currents re-sulting from tDCS are of lower amperage andare thought to modulate the resting membranepotentials of neurons rather than cause actionpotentials. Cortex near the anode, where cur-rent enters the brain, is rendered temporarilymore excitable, whereas cathodal stimulationrenders the cortex less excitable. At present thedevelopment of rTMS and tDCS protocols isbased partly on general rules of thumb concern-ing stimulation parameters (duration, intensity,and location for rTMS frequency and for tDCSpolarity) but remains largely trial and error.

Hamilton and colleagues (2011) havereviewed the prospects of noninvasive brain

stimulation for psychological enhancement ofnormal, healthy subjects. They cite researchthat has demonstrated enhancement of learn-ing and memory, including language learning,complex problem solving, and mood.

Ethical, Legal, and Societal Issuesin Brain Enhancement

Individuals, organizations, and societies havea multitude of interests that can be served byinfluencing people’s behavior, for examplemaking people (self or other) smarter, happier,more generous, or more law-abiding. Ourgrowing ability to influence normal healthybrain function is being harnessed for manyof these purposes, and this raises an array ofethical, legal, and social issues almost as diverseas the reasons for brain enhancement.

Voluntary Physician-AssistedEnhancement

Let us begin with the ethically simplest sit-uation, voluntary enhancement with medicalsupervision. Here there is no coercion andhealth risks are minimized. What is the ethicaland legal status of such a scenario, and howmight it impact society beyond the individualpatient and physician?

Concerning the physician’s role, the mainethical issue is whether physicians shouldpromote the well being of their patientsbeyond healing illness and alleviating suffering.Although other medical specialties now include“lifestyle” services such as cosmetic surgery andcosmetic dermatology, those treating the brainhave only begun to grapple with this expansionof their role. Clinicians report widely varyingattitudes toward providing their patientswith brain enhancement (Banjo et al. 2010).However, at least one professional body hasexamined the ethical issues and concluded thatthe practice is not intrinsically problematic.In a report entitled “Responding to requestsfrom adult patients for neuroenhancements,”the American Academy of Neurology’s Ethics,Law and Humanities Committee recently

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advised that it is morally and legally permissi-ble for physicians to prescribe brain-enhancingmedications to healthy individuals (Larriviereet al. 2009).

What ethical considerations apply to the in-dividual who is choosing to enhance his or herbrain? These depend in part on the psychologi-cal traits being enhanced. For example, issues ofcompetition, fairness, and freedom arise mainlyin connection with cognitive enhancement, asmental ability is a positional good as well as hav-ing value in its own right. That is, the benefitsof cognitive enhancement come in part frombeing smarter than the competition, as wellas from the inherent desirability of improvedcognition. By increasing the competitiveadvantage of some, cognitive enhancementinfluences others. In contrast, social-affectiveenhancements have relatively less-direct effectson people other than the user of the enhance-ment, so the externalities are relatively weaker.Instead, the value of authenticity and humanfeeling are the main issues that arise.

Ethical, Legal, and SocietalImplications of CognitiveEnhancement

The two main issues that arise with cognitiveenhancement are fairness and freedom. Cog-nitive enhancement has been characterized asunfair in the same way that doping in sports isunfair. Although there are similarities, the anal-ogy is imperfect for at least two reasons. First,there are reasons to enhance cognition that havenothing to do with competition, for exampleimproved understanding and increased produc-tivity, whereas performance enhancement insports is primarily for the purpose of compe-tition. Individuals who do not engage in com-petition of any kind could still have reason toenhance their cognition.

Second, even in competitive situations thepurpose of the competition is typically differentfor athletic and cognitive competitions. Forathletics, the goal is ostensibly to find outwho is the best athlete without performanceenhancement because of the value given to

athletic talent, training, and effort. For cogni-tive competitions, in contrast, we are generallyinterested in predicting future performance.Aptitude tests, such as the Scholastic Assess-ment Test and the Medical College AdmissionTest, are designed to assess capacity for successin college or medical school. Licensing examsare intended to discriminate between thosewho will and will not practice their trade or pro-fession competently. Even quizzes and examsin school are essentially means of assessing howmuch knowledge and understanding the stu-dent is likely to carry forward out of the course.

If someone routinely uses cognitive en-hancement and plans to continue doing so,then using cognitive enhancement during a testwould provide a representative estimate of hisfuture capabilities. From this perspective, en-hanced test taking is not unfair unless the testtaker plans not to use cognitive enhancementin the future.

Cognitive enhancement can also be unfairto individuals or groups who do not have accessto it. The drugs now used for this purposeare more available to the wealthier membersof society, and this seems likely to be truefor future drugs as well as devices. Cognitiveenhancement therefore has the potential toexacerbate socioeconomic disparities withinand between countries.

Finally, although cognitive enhancementcan be enabling, it can also limit individualfreedom. This could take the form of directcoercion by employers or schools. For example,it is in an employer’s interest to have workerswith enhanced attention or the ability to workthrough the night periodically. It is in a school’sinterest to have students who score well ontests and follow classroom instructions easily.Indeed, in some school districts the proportionof students on pediatrician-prescribed stimu-lant medication is higher than the prevalenceof ADHD, suggesting that enhancement istaking place (Diller 1996). Possibly in responseto schools’ conflict of interest, the U.S.government has enacted a federal law pre-venting schools from requiring treatment forADHD.

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Unfortunately, it is more difficult to leg-islate against indirect coercion, which willnaturally emerge as enhancement becomesmore common. Once a single employee wowsthe boss with the productivity made possibleby medication-enabled all-nighters, that bosswill want to encourage others to do the same.Workers may get the message that those whodo not regularly pull high-productivity all-nighters are likely to be replaced with workerswho do. As more young learners are able tosurpass expectations for classroom behaviorand academic performance, schools may raisetheir expectations, and students with averageabilities may find themselves performing belowpar if they do not engage in enhancement.

The U.S. Air Force is explicit in providingpilots with a choice concerning enhancementthat is indirectly coercive: They are toldthat they may choose whether or not to usestimulant medication on long flights, but ifthey choose not to, they may be found unfit forduty (Borin 2003). Any profession for whichwork must be performed under conditionsof distraction, sleep deprivation, or stress,especially those for which the safety of others isat stake, could become subject to such a choice.

Ethical, Legal, and SocietalImplications of Social-AffectiveEnhancement

The problems reviewed above in connec-tion with cognitive enhancement concernedrelatively pragmatic considerations of mar-ket forces, productivity, and the protection ofworkplace freedoms. Although some of thesame issues arise in connection with social-affective enhancement, as cheerful and outgo-ing individuals may be more successful in somework contexts, they are not the most obviousor pressing ones. Rather, concerns about en-hancing our emotional and social lives tend tobe more philosophical in nature, focusing onthe value of authenticity in our feelings aboutourselves, our relationships, and our world.

The enhancement of mood and personalityusing SSRIs has been criticized for distorting

our perspective on ourselves and our lives.Although few experts would discourage adepressed person from using antidepressantmedication, some see serious problems with theuse of such medications for minor mood dis-turbances or gloomy temperaments. Fukuyama(2002) has worried that SSRIs inappropriatelyraise the self-esteem of the user, thus under-mining an important source of motivation inour lives. He asks if Caesar and Napoleon wouldhave created their empires had they been able toraise their self-esteem simply by popping a pill(Fukuyama 2002, p. 46). Elliott et al. (e.g., 2004)has raised another danger of chemically inducedcontentment. Perhaps the angst or alienationwe feel about our lives is an important signalthat can prompt us to seek a more meaningfullife if it is not medicated away with an SSRI.

These critiques rest on psychologicalassumptions that, although plausible, arenot necessarily true. Does low self-esteemmotivate people to achieve greatness, or doesit more often discourage people from trying torealize their goals? Perhaps there were otherleaders and military strategists as visionary asCaesar and Napoleon, or even more so, whonever built their empires because they didnot have sufficient faith in themselves. Moregenerally, does raised self-esteem lead to moreor less self-efficacy? As for the assumptionsunderlying Elliott’s critique, it is plausible thatan increased sense of well-being might robus of the incentive to seek more meaningfulactivities and relationships or to work towarda better world, yet it might also enable us toimagine better possibilities and to have theenergy and optimism to pursue them.

The ethical, legal, and social implicationsof brain enhancement to alter interpersonalrelationships are somewhat hypothetical.On the one hand, basic research shows thatoxytocin, as well as related hormones such asvasopressin, can alter our feelings and behaviortoward others. On the other hand, the effectsof these hormones on human behavior haveonly begun to be investigated, and their effectsin different genders, individuals, and circum-stances, in combination with one another

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and with other hormones, requires moresystematic study before they form the basis ofuseful brain enhancements. In addition, thedifficulty of intranasal administration limitscurrent usefulness. This will change if drugsare developed that can cross the blood-brainbarrier to target oxytocin receptors.

In the meantime, there may be somespecial circumstances under which intranasaladministration is feasible. Anecdotal evidencesuggests that some psychiatrists use oxytocin incouples therapy (L. Young, personal commu-nication). Given the effectiveness of personalrapport and trust in obtaining informationduring interrogation, intranasal oxytocin couldbe used in law enforcement and nationalsecurity contexts (Moreno 2006). In view ofthis, Dando (2009) has called for inclusion ofoxytocin as a chemical weapon in internationallaw concerning war, for example, the GenevaConvention. With better delivery methodsor new drugs, surreptitious manipulation ofthe oxytocin system could be a profitable,if unethical, business strategy. By increasingtrust, generosity, and forgiveness in one’sopponents, one could influence the outcomesof financial, political, or other negotiations.

The ethical issues raised by relationship en-hancement are complex. Whereas drugging anunsuspecting business associate for financial ad-vantage seems clearly wrong, what if we couldobtain socially valuable information from anunwilling informant without causing physicalor psychological pain? What about encour-aging a successful resolution of difficult ne-gotiations by enhancing feelings of bondingand brotherhood in both parties? With bothparties’ informed consent?

Some commentators emphasize the ethi-cal similarity of relationship enhancement byneurochemical means and by other means(Savulescu & Sandberg 2008). From a purelyconsequentialist point of view, sufficiently highbenefits to society should tip the moral balancein favor of oxytocinizing interrogees or all par-ties in a political conflict, even without theirconsent. Yet most of us sense a troubling vi-olation of personhood in these scenarios. It is

Consequentialist:an approach to ethicswhereby the rightnessor wrongness of anaction depends solelyon the value of itsconsequences

not just the assault on autonomy inherent ininfluencing people without their knowledge; itis the co-opting of our highest moral emotionsfor instrumental purposes. After all, part of whatmakes these emotions so precious, to individu-als and society, is precisely that they guide usaway from selfishness. They shift us from thepursuit of our own selfish ends to considera-tion for the well being of others. The prospectof someone harnessing these emotions for theirown ends is therefore especially repugnant.

Similarly, involuntary enhancement ofcriminal offenders to improve their personal-ity, mood, and self-control (with SSRIs) or topromote trust and empathy for others (oxy-tocin) presents us with another set of tradeoffsbetween potentially desirable outcomes andtroubling infringement of personhood. If thesetreatments can enable offenders to live outsideof prison and can protect society againstcrime, then the “benefit” side of the equationis substantial. However, state-imposed psy-chopharmacology poses a relatively new kind oflimitation on offenders’ autonomy and privacy.In contrast to the restrictions on autonomyand privacy imposed by incarceration, whichmainly concern physical restrictions, braininterventions would restrict offenders’ abilitiesto think, feel, and react as they normally would.

THE NEUROSCIENCEWORLDVIEW

Neuroscience does not merely give us newtools to be used to the benefit or detrimentof humanity; it gives us a new way of thinkingabout humanity. The idea that human behav-ior can be understood in terms of physicalmechanisms runs counter to deeply ingrainedintuitions. Whereas we naturally think in termsof physical causality to understand the behaviorof most objects and systems in the world—whya bicycle is easier to pedal uphill in low gear,why a plant grows in the sun or withers inthe shade, why a printer jams—when it comesto human behavior we think about people’sintentions and reasons. There is evidence thateven infants understand human behavior in

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terms of intentions and reasons rather thanphysical causes (Woodward 2009).

Neuroscience provides an alternative per-spective, from which human behavior can alsobe understood as the result of physical causes.Even for people who do not follow the latesttrends in science or spend time thinking aboutthe nature of humanity, the applications of neu-roscience reviewed in the previous two sectionswill provide many reminders that our minds are,at root, physical mechanisms. By making peoplepart of the clockwork universe, neurosciencechallenges many assumptions about moralityand personhood. Three challenges are reviewedhere.

Moral Agency and Responsibility

The idea that all of our behavior, moraland immoral, is physically caused by brainprocesses throws a monkey wrench into ourintuitive reasoning about moral responsibility.We think of ourselves as moral agents whenwe act intentionally, with free will. Thus, I ammorally responsible for knocking down the oldlady if I pushed her, on purpose, to get her outof my way, but not if I stumbled or was myselfpushed and thereby pushed her because of thephysics of my body and its interactions withother parts of the scene. Far more could be saidabout the notion of free will and its relationto responsibility (e.g., see Morse 2005), but forpresent purposes the important point is thatwe are intuitively disinclined to hold someoneresponsible for an action they performed whenthe action is physically caused.

Of course, many people believe in theabstract that human behavior is physically de-termined. However, we tend to put aside suchabstractions when making moral judgments.We do not say, “But he had no choice—thelaws of physics made him do it!” However, asthe neuroscience of personality, decision mak-ing, and impulse control begins to offer a moredetailed and specific account of the physicalprocesses leading to irresponsible or crimi-nal behavior, the deterministic viewpoint willprobably gain a stronger hold on our intuitions.

Whereas the laws of physics are a little tooabstract to displace the concept of personal re-sponsibility in our minds, our moral judgmentsmight well be moved by a demonstration ofsubtle damage to prefrontal inhibitory mech-anisms wrought by, for example, past drugabuse or childhood neglect. This has alreadyhappened, to an extent, with the disease modelof drug abuse (Leshner 1997). As a resultlargely of neuroscience research showing howaddictive behavior arises from drug-inducedchanges in brain function (Rogers & Robbins2001, Verdejo-Garcı́a et al. 2004), addiction isnow viewed as more of a medical problem thana failure of personal responsibility.

Presumably because specific neuroscienceaccounts of behavior are more compellingthan generalizations about physical determin-ism, neuroimaging evidence is increasingly pre-sented by the defense during the sentencingphase of criminal trials (Hughes 2010). A studyexamining the influence of neuroscientific evi-dence in the guilt phase found that when it isincluded, judges and juries are more inclinedto find defendants not guilty by reason of in-sanity (Gurley & Marcus 2008). Outside thecourtroom, people tend to judge the behaviorof others less harshly when it is explained inlight of physiological rather than psychologicalprocesses (Monterosso et al. 2005). This is astrue for serious moral transgressions, such askilling, as for behaviors that are merely sociallyundesirable, such as overeating. The decreasedmoral stigma surrounding drug addiction is un-doubtedly due in part to our emerging view ofaddiction as a brain disease.

What about our own actions? Might anawareness of the neural causes of behavior influ-ence our own behavior? Perhaps so, accordingto a study by Vohs & Schooler (2008). Theyasked subjects to read a passage on the incom-patibility of free will and neuroscience fromFrancis Crick’s (1995) book, The AstonishingHypothesis: The Scientific Search for the Soul. Thisincluded the statement, “‘You’, your joys andyour sorrows, your memories and your ambi-tions, your sense of personal identity and freewill, are in fact no more than the behavior of

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a vast assembly of nerve cells and their asso-ciated molecules.” The researchers found thatthese people were then more likely to cheat ona computerized test than those who had read anunrelated passage.

Will neuroscience change our laws, ethics,and mores? The growing use of brain scans incourtrooms, societal precedents such as the des-tigmatization of addiction, and studies such asthose described above seem to say the answer isyes.

Religion and the Nature of Persons

Most religions endorse a two- or three-partview of the person: body and mind or soul, orbody, soul, and spirit. This accords well withmost people’s intuitions, according to whichthere is some essence of a person that is morethan just the matter that we can see and touch.Yet as neuroscience advances, all aspects of aperson are increasingly understood to be thefunctioning of a material system. This first be-came clear in the realms of perception andmotor control, where mechanistic models ofthese processes have been under developmentfor decades. Of course, such models do not seri-ously threaten the multipart view of the person:You can still believe in what Arthur Koestlercalled “the ghost in the machine” and simplyconclude that color vision and gait are featuresof the machine rather than the ghost.

However, as neuroscience begins to revealthe mechanisms of personality, love, moral-ity, and spirituality, the idea of a ghost in themachine becomes strained. Brain imaging indi-cates that all of these traits have physical cor-relates in brain function. Furthermore, phar-macologic influences on these traits, as well asthe effects of localized stimulation or damage,demonstrate that the brain processes in ques-tion are not mere correlates but are the physicalbases of these central aspects of our human per-sonhood. If these aspects of the person are allfeatures of the machine, why have a ghost at all?

By raising questions like this, it seems likelythat neuroscience will pose a far more funda-mental challenge than evolutionary biology to

many religions. After all, the genesis myth ofthe Old Testament is taken as literal truth bya relatively small number of fundamentalistChristians. In contrast, belief in an immaterialmind or soul is common to most of the world’sreligions.

Finding Meaning in a Material World

Just as we have traditionally viewed personsas different from other objects because oftheir capacity for moral agency, we have alsoviewed them as having a special moral value, asdistinct from all other kinds of objects. Personsdeserve protection from harm just becausethey are persons. Whereas we value objects forwhat they can do—a car because it transportsus, a book because it contains information,a painting because it looks beautiful—thevalue of persons transcends their abilities,knowledge, or attractiveness. Persons havewhat Kant called “dignity,” meaning a specialkind of intrinsic value that trumps the value ofany use to which they could be put (Kant 1996).

This categorical distinction between per-sons and other things is difficult to maintain ifeverything about persons arises from physicalmechanisms (Farah & Heberlein 2007). If weare really no more than physical objects, albeitvery complex objects containing powerful com-putational networks, then does it matter whatbecomes of any of us? Why should the fate ofthese objects containing human brains mattermore than the fate of other natural or man-made objects? The physicist Steven Weinberg(1993) has written, “The more the universeseems comprehensible, the more it seems point-less.” This seems an even more acute problemin neuroscience than in physics.

In sum, neuroscience is calling into ques-tion our age-old understanding of the humanperson. Much as the natural sciences becamethe dominant way of understanding the worldaround us in the eighteenth century, so neu-roscience may be responsible for changing ourunderstanding of ourselves in the twenty-firstcentury. Such a transformation could reduceus to machines in each other’s eyes, mere

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clockwork devoid of moral agency and moralvalue. Alternatively, it could help bring about asociety that is more understanding and humane

as people’s behavior is seen as part of the largerpicture of causal forces surrounding them andacting through them.

SUMMARY POINTS

1. Like genetics, neuroscience concerns the biological essence of who we are; in comparisonto genetics, neuroscience has advanced rapidly since the year 2000 and offers an array offeasible methods for predicting and controlling human behavior.

2. The newfound ability of neuroscience to explain and influence human behavior has madeit relevant to many new areas of application outside the traditional biomedical realm,including education, business, and criminal justice.

3. Brain imaging has advanced to the point where it can provide reliable information aboutthe mental traits and states of individuals in at least some circumscribed contexts.

4. The ethical, legal, and social challenge posed by progress in brain imaging is to useinformation from imaging judiciously, protecting privacy while resisting exaggeratedclaims based on the scientific aura and appeal of brain images.

5. Neurotechnologies including drugs and noninvasive brain stimulation can be used toenhance normal brain function.

6. Brain enhancement raises a host of ethical, legal, and social issues related to safety,freedom, fairness, and personal authenticity.

7. Neuroscience supports a physicalist view of the human person, according to which ourthoughts, feelings, and actions all result from physical mechanisms. This view cannoteasily be reconciled with traditional notions of moral responsibility, spirituality, andmeaning.

DISCLOSURE STATEMENT

The author is unaware of any affiliation, funding, or financial holdings that might be perceived asaffecting the objectivity of this review.

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Annual Review ofPsychology

Volume 63, 2012 Contents

Prefatory

Working Memory: Theories, Models, and ControversiesAlan Baddeley � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Developmental Psychobiology

Learning to See WordsBrian A. Wandell, Andreas M. Rauschecker, and Jason D. Yeatman � � � � � � � � � � � � � � � � � � � � �31

Memory

Remembering in Conversations: The Social Sharingand Reshaping of MemoriesWilliam Hirst and Gerald Echterhoff � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �55

Judgment and Decision Making

Experimental PhilosophyJoshua Knobe, Wesley Buckwalter, Shaun Nichols, Philip Robbins,

Hagop Sarkissian, and Tamler Sommers � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �81

Brain Imaging/Cognitive Neuroscience

Distributed Representations in Memory: Insights from FunctionalBrain ImagingJesse Rissman and Anthony D. Wagner � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 101

Neuroscience of Learning

Fear Extinction as a Model for Translational Neuroscience:Ten Years of ProgressMohammed R. Milad and Gregory J. Quirk � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 129

Comparative Psychology

The Evolutionary Origins of FriendshipRobert M. Seyfarth and Dorothy L. Cheney � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 153

Emotional, Social, and Personality Development

Religion, Morality, EvolutionPaul Bloom � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 179

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PS63-FrontMatter ARI 10 November 2011 9:52

Adulthood and Aging

Consequences of Age-Related Cognitive DeclinesTimothy Salthouse � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 201

Development in Societal Context

Child Development in the Context of Disaster, War, and Terrorism:Pathways of Risk and ResilienceAnn S. Masten and Angela J. Narayan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 227

Social Development, Social Personality, Social Motivation, Social Emotion

Social Functionality of Human EmotionPaula M. Niedenthal and Markus Brauer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 259

Social Neuroscience

Mechanisms of Social CognitionChris D. Frith and Uta Frith � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 287

Personality Processes

Personality Processes: Mechanisms by Which Personality Traits“Get Outside the Skin”Sarah E. Hampson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 315

Work Attitudes

Job AttitudesTimothy A. Judge and John D. Kammeyer-Mueller � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 341

The Individual Experience of UnemploymentConnie R. Wanberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 369

Job/Work Analysis

The Rise and Fall of Job Analysis and the Future of Work AnalysisJuan I. Sanchez and Edward L. Levine � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 397

Education of Special Populations

Rapid Automatized Naming (RAN) and Reading Fluency:Implications for Understanding and Treatment of Reading DisabilitiesElizabeth S. Norton and Maryanne Wolf � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 427

Human Abilities

IntelligenceIan J. Deary � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 453

Research Methodology

Decoding Patterns of Human Brain ActivityFrank Tong and Michael S. Pratte � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 483

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Human Intracranial Recordings and Cognitive NeuroscienceRoy Mukamel and Itzhak Fried � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 511

Sources of Method Bias in Social Science Researchand Recommendations on How to Control ItPhilip M. Podsakoff, Scott B. MacKenzie, and Nathan P. Podsakoff � � � � � � � � � � � � � � � � � � � � 539

Neuroscience Methods

Neuroethics: The Ethical, Legal, and Societal Impact of NeuroscienceMartha J. Farah � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 571

Indexes

Cumulative Index of Contributing Authors, Volumes 53–63 � � � � � � � � � � � � � � � � � � � � � � � � � � � 593

Cumulative Index of Chapter Titles, Volumes 53–63 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 598

Errata

An online log of corrections to Annual Review of Psychology articles may be found athttp://psych.AnnualReviews.org/errata.shtml

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