Kelly Burns; Antoine Bechara -- Decision Making and Free Will- A Neuroscience Perspective

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Decision Making and Free Will: A Neuroscience Perspective z Kelly Burns, J.D. y and Antoine Bechara, Ph.D. * A thorough analysis of the question of whether we possess ‘‘free will’’ requires that we take into account the process of exercising that will: that is, the neural mechanisms of decision making. Much of what we know about these mech- anisms indicates that decision making is greatly influenced by implicit processes that may not even reach conscious- ness. Moreover, there exist conditions, for example certain types of brain injury or drug addiction, in which an indi- vidual can be said to have a disorder of the will. Examples such as these demonstrate that the idea of freedom of will on which our legal system is based is not supported by the neuroscience of decision making. Using the criminal law as an example, we discuss how new discoveries in neuro- science can serve as a tool for reprioritizing our society’s legal intuitions in a way that leads us to a more effective and humane system. Copyright # 2007 John Wiley & Sons, Ltd. A visit to one of our nation’s jails or prisons will show rows of humans kept behind bars, many of whom have returned to prison on a second or third offense, committed despite their first-hand knowledge of the consequences of their actions. As a society we justify the imprisonment of such individuals by our belief that one can avoid incarceration: that someone sentenced to spend years in prison got there only through his or her own choices. That is, we possess a freedom of will, and it is misuse of that freedom that justifies restrictions on it. The question of whether we have free will, whether our actions are determined, or whether these two possibilities are even mutually exclusive, is one that continues to be debated in philosophical and scientific circles, but that obviously has important implications for the foundations of our legal system. Since the core of any free will that might exist is the ability to make choices, it is important in this debate to think about the neural mechanisms of human decision making, and whether we have absolute control over this mechanism or vice versa. Research continues to elucidate the neural processes underlying how we make our choices, and much of what we know already about these brain mechanisms indicates that decision-making is greatly Behavioral Sciences and the Law Behav. Sci. Law 25: 263–280 (2007) Published online in Wiley InterScience (www.interscience.wiley.com) DOI: 10.1002/bsl.751 * Correspondence to: Antoine Bechara, Ph.D., Hedco Neuroscience Building (HNB), Suite B26, University of Southern California, Los Angeles, CA 90089-2520, U.S.A. E-mail: [email protected] y Brain and Creativity Institute and Department of Psychology, University of Southern California. z The decision neuroscience research described in this article was supported by NIDA grants DA11779-02, DA12487-03, DA16708, and by NINDS grant NS19632-23. Copyright # 2007 John Wiley & Sons, Ltd.

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Transcript of Kelly Burns; Antoine Bechara -- Decision Making and Free Will- A Neuroscience Perspective

  • Decision Making and Free Will:A Neuroscience Perspectivez

    Kelly Burns, J.D.y and Antoine Bechara, Ph.D.*

    A thorough analysis of the question of whether we possessfree will requires that we take into account the process ofexercising that will: that is, the neural mechanisms ofdecisionmaking.Much of what we know about thesemech-anisms indicates that decisionmaking is greatly inuencedby implicit processes that may not even reach conscious-ness. Moreover, there exist conditions, for example certaintypes of brain injury or drug addiction, in which an indi-vidual can be said to have a disorder of the will. Examplessuch as these demonstrate that the idea of freedom of willon which our legal system is based is not supported by theneuroscience of decisionmaking. Using the criminal law asan example, we discuss how new discoveries in neuro-science can serve as a tool for reprioritizing our societyslegal intuitions in away that leads us to amore effective andhumane system. Copyright# 2007 JohnWiley & Sons, Ltd.

    A visit to one of our nations jails or prisons will show rows of humans kept behind

    bars, many of whom have returned to prison on a second or third offense, committed

    despite their rst-hand knowledge of the consequences of their actions. As a society

    we justify the imprisonment of such individuals by our belief that one can avoid

    incarceration: that someone sentenced to spend years in prison got there only

    through his or her own choices. That is, we possess a freedom of will, and it is misuse

    of that freedom that justies restrictions on it.

    The question of whether we have free will, whether our actions are determined, or

    whether these two possibilities are even mutually exclusive, is one that continues to

    be debated in philosophical and scientic circles, but that obviously has important

    implications for the foundations of our legal system. Since the core of any free will

    that might exist is the ability to make choices, it is important in this debate to think

    about the neural mechanisms of human decision making, and whether we have

    absolute control over this mechanism or vice versa. Research continues to elucidate

    the neural processes underlying how we make our choices, and much of what we

    know already about these brainmechanisms indicates that decision-making is greatly

    Behavioral Sciences and the Law

    Behav. Sci. Law 25: 263280 (2007)Published online in Wiley InterScience

    (www.interscience.wiley.com) DOI: 10.1002/bsl.751

    *Correspondence to: Antoine Bechara, Ph.D., Hedco Neuroscience Building (HNB), Suite B26,University of Southern California, Los Angeles, CA 90089-2520, U.S.A. E-mail: [email protected] and Creativity Institute and Department of Psychology, University of Southern California.zThe decision neuroscience research described in this article was supported byNIDAgrantsDA11779-02,DA12487-03, DA16708, and by NINDS grant NS19632-23.

    Copyright # 2007 John Wiley & Sons, Ltd.

  • inuenced by implicit processes that do not necessarily reach consciousness.

    Furthermore, neurological evidence suggests that focal brain damage can disturb the

    normal operation of some of these implicit processes. In such cases the individual

    begins to appear as if aficted with a disorder of his or her will, as evidenced by

    repeated decisions and actions that are against the persons best interests, and failure

    to learn from repeated mistakes, in spite of perfectly intact intellect, memory and

    other cognitions (Bechara, 2003). Thus neuroscience brings us evidence that

    questions the idea, which the law assumes, that free will is always intact, and as

    long as one is cognitively normal, there is no excuse for a person not to be able to

    choose between right and wrong.

    While recognizing that the continuing free will versus determinism controversy

    makes condent acceptance of either idea naive, the legal system nonetheless has

    remained attached to the notion of free will as necessary, in its view, for the

    maintenance of social order (Cotton, 2005). The SupremeCourt even has called free

    will a universal and persistent foundation stone in our system of law, as

    compared with a deterministic view of human conduct that is inconsistent with the

    underlying precepts of our criminal justice system (United States v. Grayson, 1978).

    Several scholars have argued (Cotton, 2005; Greene & Cohen, 2004; Jones, 2003),

    however, that neuroscience or other research that seems to undermine the notion of

    free will need not be seen as such a threat to our legal system. Rather, this research

    provides an opportunity for our society to reexamine the underpinnings of the legal

    system, and reprioritize in a way that is more responsive to the facts of human biology

    and psychology, and thus more effective.

    The following section of this article will outline features of the neuroscience of

    decision making that bear upon the question of whether humans have free will. We

    will discuss the normal decision-making process, and also focus on a few examples

    where this process has been known to break down. In the next section we will explore

    the implications of this research for the legal system. While more research is needed

    to fully understand the mechanisms of will, what we already know can hopefully

    inspire some creative solutions to the societal problems that the legal system

    addresses.

    THE NEUROSCIENCE OF DECISION MAKINGAND WILLPOWER

    Willpower, as dened by the Encarta1 World English Dictionary (2006), is a

    combination of determination and self-discipline that enables somebody to do

    something despite the difculties involved. This is the mechanism that enables one

    to endure sacrices now in order to obtain benets later. Otherwise, how would one

    accept the pain of surgery? Why would someone resist the temptation to have

    something irresistible, or delay the gratication from something that is appealing?

    We will argue that these complex and apparently indeterminist behaviors are the

    product of a complex cognitive process sub-served by two separate, but interacting,

    neural systems: (1) an impulsive, amygdala-dependent, neural system for signaling

    the pain or pleasure of the immediate prospects of an option, and (2) a reective,

    prefrontal-dependent, neural system for signaling the pain or pleasure of the future

    prospects of an option. The nal decision is determined by the relative strengths of

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    264 K. Burns and A. Bechara

  • the pain or pleasure signals associated with immediate or future prospects. When the

    immediate prospect is unpleasant, but the future is more pleasant, then the positive

    signal of future prospects forms the basis for enduring the unpleasantness of

    immediate prospects. This also occurs when the future prospect is even more

    pleasant than the immediate one. Otherwise, the immediate prospects predominate,

    and decisions shift towards short-term horizons. As suggested by Damasio (1994),

    willpower is just another name for the idea of choosing according to long-term

    outcomes rather than short-term ones.

    We have used the term somatic (Damasio, 1994) to refer to the collection of

    body-related responses that hallmark these affective and emotional responses.

    Somatic refers to the Greek word soma, i.e. body. Although during the process of

    weighing somatic (affective) responses the immediate and future prospects of an

    optionmay trigger numerous somatic responses that conict with each other, the end

    result is that an overall positive or negative somatic state emerges. We have proposed

    that the mechanisms that determine the nature of this overall somatic state (i.e.

    positive or negative) are consistent with the principles of natural selection, i.e.

    survival of the ttest (Bechara & Damasio, 2005). In other words, numerous and

    often conicting somatic states may be triggered at the same time, but stronger ones

    gain selective advantage over weaker ones. With each thought brought to working

    memory, the strength of the somatic state triggered by this thought determines

    whether the same thought is likely to recur (i.e. will be brought back to memory so

    that it triggers another somatic state that reinforces the previous one), or whether the

    thought is likely to be eliminated. Thus over the course of pondering a decision,

    positive and negative somatic markers that are strong are reinforced, while weak ones

    are eliminated. This process of elimination can be very fast. Ultimately, a winner

    takes all; an overall, more dominant, somatic state emerges (a gut feeling or a

    hunch so to speak), which then provides signals to the brain that modulate activity

    in neural structures involved in biasing decisions. This winner takes all view is

    consistent with the conception by Strack andDeutsch of competition betweenmotor

    schemata (Strack & Deutsch, 2004).

    The Somatic Marker Framework

    The somatic marker framework provides a system-level neuroanatomical and

    cognitive framework for decision making, and for choosing according to long-term

    outcomes rather than short-term ones. It suggests that the process of decision

    making depends in many important ways on neural substrates that regulate

    homeostasis, emotion and feeling (Damasio, 1994).

    Somatic states can be induced from (1) primary inducers and (2) secondary

    inducers (Damasio, 1995). Primary inducers are innate or learned stimuli that cause

    pleasurable or aversive states. Once present in the immediate environment, they

    automatically and obligatorily elicit a somatic response. The actual encounter of a

    drug by an addicted individual is an example of a primary inducer (Bechara,

    Damasio, & Damasio, 2003). Secondary inducers, on the other hand, are entities

    generated by the recall of a personal or hypothetical emotional event, i.e. thoughts

    and memories of the primary inducer, which elicit a somatic response. The recall

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    Decision making and free will 265

  • or imagination of a drug experience by an addicted individual is one example of a

    secondary inducer (Bechara et al., 2003).

    We have argued that the amygdala is a critical substrate in the neural system

    necessary for triggering somatic states from primary inducers. It couples the features

    of a primary inducer with the somatic state associated with the inducer. This somatic

    state is evoked via effector structures such as the hypothalamus and autonomic

    brainstem nuclei that produce changes in internal milieu and visceral structures

    along with other effector structures such as the ventral striatum, periaqueductal gray

    (PAG), and other brainstem nuclei, which produce changes in facial expression and

    specic approach or withdrawal behaviors. The amygdala is one of our evolutionarily

    older brain structures, located deep in the medial temporal lobes. Once somatic

    states from primary inducers are induced, signals from these somatic states are

    relayed to the brain stem and forebrain. Signals from activated somatic states lead to

    the development of somatic state patterns in the brainstem (the evolutionary oldest

    areas of the brain) or the cortex (the evolutionary newer areas). The perception of

    these patterns at the brainstem level is by and large unconscious, but at the level of

    the cortex this perception may become conscious in the form of a subjective feeling.

    After a somatic state has been triggered by a primary inducer and experienced at

    least once, a pattern for this somatic state is formed. The subsequent presentation of

    a stimulus that evokesmemories about a specic primary inducer will then operate as

    a secondary inducer. Secondary inducers are presumed to re-activate the pattern of

    somatic state belonging to a specic primary inducer. For example, recalling or

    imagining the experience of a drug re-activates the pattern of the somatic state

    belonging to the actual previous encounter of that drug. However, the somatic state

    generated by the recall or imagination of using a drug (secondary inducer) is usually

    fainter than one triggered by an actual use of that drug (primary inducer). The

    prefrontal cortex is a brain structure that is both evolutionarily recent and one of the

    last structures to develop fully over an individuals lifespan.

    Non-conscious Operation of Somatic States

    During the pondering of a decision, somatic states are triggered by primary or

    secondary inducers. Once induced, they participate in two functions. In one they

    provide a substrate for feeling the induced state. In the other they provide a substrate

    for inuencing or biasing decisions. Most intriguing is that the presence of these

    somatic states and their inuence on decision making and behavior need not be

    conscious.

    A study using the Iowa Gambling Task illustrates this point (Bechara, Damasio,

    Tranel & Damasio, 1997). In the Iowa Gambling Task, subjects are given four decks

    of cards and $2000 in play money with which to play a game, and are instructed that

    their goal in the game is to win asmuchmoney as possible. Each time a subject selects

    a card, she or he either wins or loses some amount of money. Decks A and B are

    disadvantageous decks, where the immediate reward is higher ($100 per card) but

    the losses are large, and playing more often from these decks leads to an overall loss.

    Decks C and D are advantageous, drawing lower rewards per card ($50), but with

    smaller penalties such that playing mostly from these decks leads to an overall gain.

    While each subject plays the game, measures are taken of skin conductance

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    266 K. Burns and A. Bechara

  • responses (SCRs) to test their non-conscious responses to making card choices.

    Subjects are also asked at intervals during the game whether they understand what is

    going on in the game, to compare their conscious development of strategy to any

    unconscious strategizing that might be underway.

    The results of this experiment demonstrate the operation of covert somatic states

    in biasing decisions. In the Iowa Gambling Task, normal subjects began to select

    advantageously before they consciously developed an understanding of which decks

    were advantageous. In addition, these subjects generated an anticipatory SCR before

    choosing a card from the disadvantageous decks, and likewise started generating this

    response before having conceptualized that these decks were disadvantageous.

    Responses can be broken down further into four stages. In the pre-punishment

    stage, before encountering losses, subjects preferred the higher-gain decks. In the

    pre-hunch stage, subjects began to generate SCRs to decks A and B, but all

    indicated that they had no clue what was going on in the game. All normal subjects

    expressed a hunch by about card 50 that A and B were riskier; we called this the

    hunch stage. Eventually most normal subjects expressed an understanding of

    which decks were riskier (this was usually by about card 80), in what we called the

    conceptual period. Notably, even subjects who never reached the conceptual

    period actually made advantageous choices in playing.

    The fact that normal subjects can make advantageous choices without having the

    factual knowledge required to logically support those choices has interesting

    implications for our understanding of the decision making process and free will.

    Research indicates that in the striatum somatic states operate implicitly, using

    knowledge without awareness. Other areas of the brain (the anterior cingulate,

    and perhaps the adjacent supplementary motor area) bias decision making using

    knowledge with awareness; that is, they engage in our common-sense version of

    the decision-making process using conscious and explicit knowledge of a decisions

    consequences. So while both conscious and unconscious knowledge are contributing

    to the process of choice, the fact that the generation of somatic states can guide us

    toward benecial behaviors without any input from our conscious deliberations

    indicates that much behavior that seems to be free will may be determined by the

    routine operation of a healthy neural mechanism. What happens when something

    goes wrong with this process elucidates this point further.

    Neural Mechanisms of Willpower

    Based on the somatic marker framework, we have proposed that willpower (or lack

    thereof) emerges from the dynamic interaction between two separate, but

    interacting, neural systems: (1) an impulsive system that triggers somatic states

    from primary inducers and (2) a reective system that triggers somatic states from

    secondary inducers. The reective system controls the impulsive system via several

    mechanisms of impulse control. However, this control of the reective system is not

    absolute: Hyperactivity of the impulsive system can overwhelm or hijack the

    inuence of the reective system.

    It is important to note that at the process level the characteristics of the

    impulsive and reective neural systems are similar to the two-system view of

    Kahneman and Tversky on intuition versus reasoning (Kahneman & Tversky,

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    Decision making and free will 267

  • 1979), or that of Strack and Deutsch on reective and impulsive determinants of

    social behavior (Strack & Deutsch, 2004). In all cases, the distinction is between the

    operations of one system that are typically fast, automatic, effortless, implicit and

    habitual, and the operations of another system that are slow, deliberate, effortful,

    explicit and rule governed. The distinct characteristic of our view is the assignment

    of neural substrates and physiological mechanisms for the operations of these

    systems.

    More specically, exposure to primary inducers (e.g. drugs) triggers fast,

    automatic, and obligatory somatic states via the amygdala system. Somatic states

    triggered by the amygdala are short lived and habituate very quickly (Buchel, Morris,

    Dolan, & Friston, 1998; Dolan et al., 1996; LaBar, Gatenby, Gore, LeDoux, &

    Phelps, 1998). Secondary inducers trigger somatic states via the ventromedial

    prefrontal cortex from perceived or recalled mental images. While the amygdala is

    engaged in emotional situations requiring a rapid response, i.e. low-order

    emotional reactions arising from relatively automatic processes (Berkowitz, 1993;

    LeDoux, 1996), the ventromedial prefrontal cortex is engaged in emotional

    situations driven by thoughts and reection. Once this initial amygdala emotional

    response is over, high-order emotional reactions begin to arise from relatively

    more controlled, higher-order processes involved in thinking, reasoning and

    consciousness (Schneider & Shiffrin, 1977). Unlike the amygdala response, which is

    sudden and habituates quickly, the ventromedial prefrontal cortex response is

    deliberate, slow, and lasts for a long time. Thus the prefrontal cortex helps predict

    the emotion of the future, thereby forecasting the consequences of ones own actions

    (see Figure 1).

    Once somatic states are triggered via the amygdala or the prefrontal cortex, a

    large number of channels can then convey body information to the central nervous

    system (e.g. spinal cord and vagus nerve). Furthermore, early evidence suggests

    that the biasing action of somatic states on behavior and cognition is mediated, at

    least in part, by the release of neurotransmitters, such as the neurotransmitters

    dopamine (DA), serotonin (5-HT), noradrenaline (NA) and acetylcholine (Ach).

    Indeed, the neurons that manufacture these neurotransmitters are situated in

    such a way that, on one end (the dendrite end), they can convey somatic state

    signals, which then inuence the pattern of neurotransmitter release at the other

    end (the axon terminals end). In turn, changes in neurotransmitter release can

    modulate synaptic activities of neurons subserving behavior and cognition within

    the reective system. This chain of neural mechanisms provides a way for somatic

    states to inuence activity in a variety of neural regions important for decision

    making. Thus the signicance of this neural arrangement is that, regardless of how

    somatic states are triggered, i.e. impulsively (primary induction) or reectively

    (secondary induction), once they are triggered, they can gain access to cortical and

    subcortical neurons subserving cognition. Thus, depending on their strength, they

    have the capacity to modify and inuence cognition, especially decision making

    (see Figure 1).

    Early in life, the reective system is poorly developed and willpower is relatively

    weak. Behavior is more dominated by the impulsive systemchildren tend to

    behave in a manner that they do what they feel like doing right now, without much

    thought about the future. However, through learning they learn to constrain many

    desires and behaviors that conict with social rules, and that lead to negative

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    268 K. Burns and A. Bechara

  • consequences. This is the rst sign of the development of willpower, and an example

    of how the reective system gains control over the impulsive system. This ability, i.e.

    to choose according to long-term outcomes, and resist immediate desires, requires

    the normal development and normal triggering of somatic states by the reective

    system, which signal the value of long-term outcomes. Deprived of these somatic

    states, the reective system loses its control, and willpower breaks down. Indeed, this

    is exactly what happens when areas of the ventromedial prefrontal cortex are

    damaged.However, it appears that there is more than onemechanism through which

    the reective system exerts control over the impulsive system.

    The functional evolution of the prefrontal cortex appears to involve an

    incremental increase in its capacity to access representations of events that occur

    in the more distant future. This enhanced futuristic capacity coincides with the

    development of more rostral/anterior regions of the ventromedial prefrontal cortex.

    Comparative studies of the frontal lobes in humans and non-human primates have

    revealed that the major advancement in the size, complexity and connectivity of the

    frontal lobes in humans relates primarily to Brodmann Area 10, i.e. the frontal pole

    (Semendeferi, Armstrong, Schleicher, Zilles, & Van Hoesen, 2001), and not so

    much to the more posterior areas of the ventromedial prefrontal cortex

    (Semendeferi, Lu, Schenker, & Damasio, 2002). For this reason, we have argued

    that there is a distinction between two broadmechanisms of behavioral and cognitive

    control.

    (1) Decision making, which reects a tendency to think about the consequences of a

    planned act before engaging in that act. It requires knowledge about facts and values,

    and it involves conscious, slow and effortful deliberation about consequences that

    may or may not happen in a distant future. An example requiring decision making is

    nding a briefcase containing $100 000 in a dark alley. The decision to take or not

    take the money may require some deliberation about the ethics, morality and

    consequences of such an action. The critical neural region for this mechanism of

    control is the more anterior region of the ventromedial prefrontal cortex, i.e. that

    involving the frontal pole and Brodmann Area 10 (Bechara, 2004). This area is

    particularly the cortex area that has evolved so much further in humans than in other

    animals, including non-human primates, and this gives us distinguishing cognitive

    abilities such as projecting into the future, understanding probabilities and having

    the ability to decide and act upon them, and being motivated by abstract principles

    beyond daily survival needs.

    (2) Impulse control reects inhibition of a pre-potent act (motor impulse control), or a

    pre-potent mental image/thought (attentional impulse control). The learning to quickly

    and automatically inhibit such a pre-potent act (or thought) is due, in large part, to

    the triggering of a somatic state, which signals the immediate and certain nature

    of the consequences. An example of this quick, automatic and implicit mechanism

    of impulse control is nding a similar amount of $100,000 spread out on a table

    inside a bank. Normally, any thought, intention or impulse to grab the money is

    inhibited automatically and effortlessly. The critical neural region for the

    mechanism of motor impulse control is the more posterior region of the

    ventromedial prefrontal cortex, i.e. that involving the anterior cingulate (Bechara,

    2003, 2004). The critical neural region for the mechanism of attentional impulse

    control is the lateral orbitofrontal and dorsolateral (inferior frontal gyrus) region

    (Bechara, 2003, 2004).

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    Decision making and free will 269

  • Loss of Willpower

    The complex system that we have outlined above carries with it several distinct but

    interrelated ways in which it can fail or be compromised. Choosing according to

    long-term outcomes rather than short-term ones requires that the somatic states

    triggered by the reective system dominate those triggered by the impulsive system.

    Two broad types of condition could alter this relationship and lead to loss of

    willpower: (1) a dysfunctional reective system and (2) a hyperactive impulsive

    system. The neural regions of the reective system, which exert top-down control

    on decision making (anterior ventromedial prefrontal cortex), motor impulse control

    (anterior cingulate), and perceptual impulse control (lateral orbitofrontal and

    dorsolateral), are all targets for the neural systems that convey bottom-up

    inuence of somatic signals. The inuence of these somatic signals could be

    non-conscious and implicit, or conscious and explicit, i.e. accompanied by a certain

    feeling of urge. The example of substance dependence, and our research with

    dependent individuals, demonstrates how various dysfunctions can affect this

    process.

    Reective System Dysfunction

    Our research has demonstrated that individuals who are substance dependent, or

    those who have suffered bilateral damage to the ventromedial prefrontal cortex, show

    similar behavior patterns related to dysfunction of the reective system. Two

    characteristics in particular are relevant to this discussion. First, both groups often

    are in denial or unaware that they have any problem. Second, individuals in both

    groups tend to act in such a way that brings about immediate reward, even when that

    comes at the risk of incurring extremely negative future consequences, which may

    include loss of job, home, important life relationships, and reputation, and often

    troubles with the law. Such individuals act seemingly in ignorance of this risk.

    Examples of this pattern related to substance use cause family strife nationwide and

    can be seen in the newspapers every day. The most famous case of prefrontal cortex

    injury, if not the most famous case in neuroscience, is that of Phineas Gage. In 1848,

    Gage survived a freak construction accident that sent a metal rod through his brain,

    obliterating his ventromedial prefrontal cortex without ever causing loss of

    consciousness. Gages life functions and intellect were miraculously unaffected

    by the injury. However, his co-workers described him after the injury as no longer

    Gage, seeing that a man who once had been responsible and a role model for other

    workers had become obnoxious, crass, and foolish, and able to behave only in ways

    that were sure to bring about personal ruin.

    Though at the time of Gages injury the neural reasons for this personality change

    were unknown, modern neuroscience explains how his cognitive processes had been

    disturbed. While normal subjects executing the Iowa Gambling Task generate SCRs

    while they consider drawing a card from a disadvantageous deck, subjects with

    bilateral prefrontal damage do not generate this response (Bechara et al., 1997). In

    other words, their reective systems are not generating somatic states that help bias

    the response away from disadvantageous decisions. The outcomes of these subjects

    decisions are as wemight expect: They do not begin to choose advantageously during

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    270 K. Burns and A. Bechara

  • the pre-hunch or hunch periods. In fact, these subjects do not even choose

    advantageously when they reach the conceptual period, despite the fact that, when

    asked, they describe with accuracy what strategy will win the game! Substance

    dependent subjects behave on the Iowa Gambling Task just as prefrontal cortex

    lesion patients do, and also do not generate SCRs biasing them away from bad

    decisions (Bechara, Dolan, & Hindes, 2002). Research in which substance

    dependent subjects executed other, similar decision-making tasks has yielded

    similar results (Bartzokis et al., 2000; Grant, Bonson, Contoreggi, & London, 1999;

    Grant, Contoreggi, & London, 1997, 2000; Mazas, Finn, & Steinmetz, 2000; Petry,

    Bickel, & Arnett, 1998; Rogers et al., 1999).

    The absence of somatic response is an example of a dysfunction in the

    decision-making control mechanisms. The reective system can also exhibit a failure

    or disability in its perceptual or motor impulse control mechanisms. Again using

    substance abuse as an example, a substance dependent person might be unable to

    suppress the thought of taking the drug, if perceptual control is faulty. If the decit is

    in motor impulse control, the person might act so quickly in response to the drug

    stimulus that the person does not even have a chance to think about it.

    One way to test impulse control mechanisms is to ask subjects to perform tasks in

    response to changing stimuli, and measure their response times. For example, in the

    stop-signal paradigm, subjects are shown left and right pointing arrows and are asked

    to respond to the arrows, but to inhibit their response when the color of the arrow

    changes (the stop signal). The color changes come occasionally but unpredic-

    tably.When this experiment was performed, substance dependent subjects exhibited

    quicker response times than normal controls, but signicantly longer response times

    to the stop signal, reecting problems with impulse control (Crone, Cutshall,

    Recknor, Van den Wildenberg, & Bechara, 2003). Other studies also have

    demonstrated difculties of impulse control associated with drug and alcohol

    addiction(Crone et al., 2003; Noel, Van Der Linden, Verbanck, Pelc, & Bechara,

    2003; Noel, Van Der Linden, Verbanck, Pelc, & Bechara, 2005).

    Impulsive System Hyperactivity

    It is also possible for the impulsive system to exaggerate the somatic response of

    reward stimuli, resulting in it becoming exceedingly difcult for even a well

    functioning reective system to generate somatic responses that bias the person

    toward inhibiting action, or executing will. We might conceptualize this as a

    hijacking of the execution of willpower by an overactive impulsive system, where

    will becomes guided by the amygdala rather than by the prefrontal cortex. Research

    using varieties of the Iowa Gambling Task has shown exactly this hypersensitivity to

    reward in substance dependent subjects. In one experiment, skin conductance

    responses in substance dependent subjects were higher in magnitude when

    anticipating rewards as compared with normal controls, whereas SCRs when

    anticipating punishments were relatively weak (Bechara et al., 2003, 2002). This

    concept of impulse control is also supported broadly by some of the prominent work

    on impulsivity, such as that by Moeller, Barratt, Swann, and their colleagues

    (Moeller, Barratt, Dougherty, Schmitz, & Swann, 2001).

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    Decision making and free will 271

  • We have used the example of substance dependence as an illustration of the ways

    in which decision-making processes can be compromised. It is important to note that

    we are not making any assertions about the roots of substance dependence or coming

    to conclusions about whether decision-making impairments are a cause or a result of

    the prolonged substance use. Rather, this explanation serves to highlight the

    similarities between substance dependent persons and individuals with prefrontal

    cortex damage in executing decision-related tasks about subjects that are unrelated

    to substance use. The high degree of similarity indicates that, regardless of cause or

    prognosis, both populations serve as good examples of what can go wrong in decision

    processing, and therefore shed light on what is happening in all cases of

    decision-making functioning.

    So do we Have Free Will?

    Given all of this information about the neural mechanisms of human decision

    making and some of the ways these mechanisms can go awry, what does this tell us

    about whether we have free will, and how the legal system should deal with this?

    Really, this breaks down into two, related questions. (1) Does the average human

    have free will? (2) Does the average person who becomes involved with the legal

    system have free will? A negative answer to either of these questions requires us to

    revisit the strong assumptions of free will under which our legal system operates.

    The second question is perhaps easier to address, as much of the research cited

    above is directly pertinent to this question. Though it is by no means true that all

    people who commit crimes are substance dependent or mentally ill, the fact that

    substance abuse and mental illness plays a role in the behavior of a large percentage

    of offenders is undeniable. To consider just one statistic on this relationship, the

    Bureau of Justice Statistics reports that in 2002, 68% of jail inmates reported having

    symptoms that satised the criteria for the DSM IV denition of substance

    dependence during the year prior to their admission to jail (Substance Dependence,

    Use, and Treatment of Jail Inmates, 2002). Our research has shown that substance

    dependence is associated with impairment of the neural processes subserving

    decision making and that this impairment is global (i.e., it applies to many decisions,

    not only decisions about whether to engage in substance use) (Breiter, Aharon,

    Kahneman, Dale, & Shizgal, 2001; Breiter & Rosen, 1999). Therefore, well over half

    of people who are arrested and held in jails may be operating with an ability to decide

    and exercise willpower that is lower than that of the average person.

    It is important to note, however, that there is muchmore research that needs to be

    done regarding the neuroscience of human decision making, and while substance

    dependence is a relatively easy condition to identify and test it is only one example of

    a neurological prole that results in decreased decision-making capacity. This point

    is demonstrated by our recent work comparing the decision-making proles of

    inmates convicted of different criminal offenses with each other, and with the proles

    of normal controls, substance dependent subjects, and orbitofrontal cortex lesion

    patients. We found that the proles of individuals convicted of drug, sex, theft and

    intoxicated driving offenses mirrored those of substance dependent subjects, while

    the proles of those convicted of assault and murder resembled the proles of brain

    lesion patients (Yechiam et al., 2006). The research revealed this pattern, but was

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    272 K. Burns and A. Bechara

  • not designed to assess why this result occurred, and thus leaves many questions open

    for further study (e.g. At what point in the lives of these offenders did this prole

    emerge? Due to what causes? What role did substance use by the offenders play in

    creating these proles? Why is it not then true that all brain lesion patients go on to

    commit violent crimes? etc.). What is important to note for the purposes of this

    article is that this pattern does exist, leaving us both with evidence that many more

    people involved in the justice system may have gotten there operating with faulty

    neural mechanisms, and that similar impairments may exist in other, as yet

    unidentied, population subgroups that are also operating with less than full free will,

    by any denition.

    This understanding applies as well when we are talking about non-offender

    populations: Can we say, knowing what we do about the neural mechanisms of

    choice in healthy adults, that our choice is free? As stated above, there are many

    further avenues for research that will continue to teach us about the neuroscience of

    willpower, and with those discoveries still in the future, we are reluctant to issue a

    gross statement declaring that we do or do not have free will. Particularly relevant for

    the issue of legal responsibility, more research could be done regarding the

    decision-making processes in healthy individuals who are under stress, as is often the

    case when choices that result in legal system involvement occur. We have focused

    thus far on individuals who are across the board normal, or who are subject to

    conditions such as substance dependence or neurological disorder that affect them at

    all times. A full understanding of the operation of the process of choice will include

    the various states of mood, health and environment through which all human beings

    cycle. As is the case in most disciplines, there is likely to be a continuum of

    impairment in the exercise of willpower rather than a black-or-white state of

    dysfunction or health.

    This said, what we do know about the process of choice indicates that there is a

    strong deterministic element to actions that appear to us to be indeterminist or freely

    chosen. The exceptions, noted above, of impairments of willpower prove the rule

    that our exercise of will, presumably in the service of being able to survive and thrive,

    is inuenced in large part by the automatic and involuntary functioning of particular

    neural pathways. Recalling our discussion of the Iowa Gambling Task, lesion

    patients who could accurately explain to researchers what a winning strategy for the

    game was were nonetheless unable, due to neurological decit, to follow that

    strategy. This phenomenon demonstrates that it is more than an intellectual

    understanding of consequences, morals and ethics that guides a persons actual

    behavior in the real world. It is also the operation of neural mechanisms that generate

    somatic states, automatically and obligatorily, that exert enough of a bias on behavior

    to render irrelevant the ability to know one should behave otherwise. What states

    are actually generated depends on a complex network of all the stimuli a person has

    ever encountered, all the responses she or he has ever had to those stimuli, and all the

    brain patterns that these stimulusresponse pairings have created.

    Perhaps, then, the most important question is yet a third one: Do we possess the

    kind of free will that justies not only legal responsibility, but the stigma and

    disapprobation that are associated with failures to conform to societys laws? The

    compassionate answer to this question must be no. How this might play out in a

    reexamination of our societal assumptions is the subject of the next section of this

    article.

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    Decision making and free will 273

  • LEGAL IMPLICATIONS OF THE NEUROSCIENCE OFDECISION MAKING: HOPES AND DIRECTIONS FOR

    FUTURE INTERDISCIPLINARY RESEARCH

    Before moving on, it is a good time to take note that although the examples we have

    used so far, and on which we will continue to focus, come from criminal law,

    decision-making research and what it reveals about free will has implications inmany

    areas of the law. Contract law, for example, is based on the premise that two or more

    parties can decide upon a course of action and make commitments to each other to

    follow rules of interaction that they set out for their relationship, and tort laws

    emphasis on duty and negligence presupposes some ability to control ones behavior.

    The criminal law example is perhaps particularly compelling because it is in criminal

    law alone that the assumption of freedom of choice justies relieving citizens of their

    basic rights to liberty or even life. However, the call for society to view those who

    break the law with understanding applies whether they violate criminal prohibitions,

    contract provisions or duties of care to their fellow citizens.

    Though courts embracing free will have done so because they have deemed it a

    necessary assumption for an operable justice system, most scholars who have

    addressed the issue have agreed that any scientic discoveries that undermine free

    will do not therefore undermine all the foundations on which the criminal legal

    system is based. Rather, they call for a reprioritization of values, better alignment

    between the stated and actual reasons for the systems character, or a commitment to

    resolving some of the tensions that are already at play in the system and are only

    highlighted, not created, by discoveries in the social and biological sciences (Cotton,

    2005; Greene & Cohen, 2004; Jones, 2003). Examination of the four justications

    for punishmentdeterrence, incapacitation, rehabilitation, and retributionin

    light of decision-making neuroscience lends further support to this way of

    approaching the issue.

    The Tenability of our Justications for Punishment

    Each of the four classic justications for punishment expresses at least one facet of

    the collection of interests that come into contact in the justice system. Since many of

    these interests focus on theories of how to inuence choice, or what is the correct

    ethical response to bad choices that harm others, the research cited in this paper on

    the neuroscience of choice has obvious implications for several of these justications.

    Indeed, rather than threatening the foundations of the system, it is our hope that the

    research and its implications can be seen as a means to harmonize these justications

    into a more unied and workable whole by inspiring further research into the many

    unanswered questions that remain to be answered as neuroscience researchers focus

    more closely on forensic populations.

    Retribution

    The retributive impulse behind the features of the criminal justice system are

    evident, if not in the facts of the system itself, then in the rhetoric of tough on

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    274 K. Burns and A. Bechara

  • crime political platforms and the ever-increasing harshness of proposed sentencing

    and other criminal legislation. Some scholars credit retribution as being the primary

    justication for punishment, as it is the one that best explains the actual features of

    the system currently in operation (Greene & Cohen, 2004, pp. 17761777). Yet it is

    perhaps the justication most undermined by any hypothesis of limited free will,

    because who deserves punishment for the involuntarily action of neural

    mechanisms?

    Greene and Cohen provide a thorough analysis of this point in a recent article,

    concluding that as advances in neuroscience reveal more about the mechanistic

    nature of decision making, individuals in society will cling less rmly to their

    retributive impulses and beliefs. Moreover, as more individual attitudes change, so

    will the law. In their words, The law will continue to punish misdeeds, as it must for

    practical reasons, but the idea of distinguishing the truly, deeply guilty from those

    who are merely victims of neuronal circumstances will, we submit, seem pointless

    (Greene & Cohen, 2004, p. 1781). We believe that the decision-making processes

    discussed in this article exemplify exactly the type of discovery to which Greene and

    Cohen refer in their work, and that the implications are indeed as they predict.

    That the moral intuitions and commitments (Greene & Cohen, 2004, p. 1778)

    of society are changing in this way can be seen in the tensions that already exist in the

    system as it is. Michelle Cotton, in another recent paper, outlines the historical

    incursions determinism hasmade into the courtroom, driven by sympathies for those

    who wind up in court due to behaviors that only make sense given their respective

    mental developmental states (e.g. the mentally ill, youth, intoxicated persons). In

    most areas, however, with some exceptions in juvenile law and the insanity defense,1

    Cotton contends that the fear of the slippery slope led courts and legislatures to

    banish any vestiges of determinism from our practical philosophy of criminal

    responsibility. The result is what she calls a foolish consistency, which does not

    take the realities of human psychology into account, and thus leaves us with a system

    that neither inspires condence nor achieves results (Cotton, 2005).

    There is further tension between the sympathy that new understandings of human

    behavior engender, and the retributive impulse that is not just a principle of law but is

    itself a psychological phenomenon. Matthew Jones notes, in a piece discussing the

    impact of genetics research on the law, that legal scholars predicting the end to the

    current criminal justice system are misguided . . . [because] they do not take intoaccount the considerable role that punishment plays in acting as both a healing

    device and an outlet for revenge (Jones, 2003). Greene and Cohen, while

    expressing optimism that society can learn to move past the retributive impulse, cite

    recent primate studies demonstrating that revenge, or a sense of justice, might

    inherently be with us from our evolutionary beginnings, presumably having aided the

    survival of the species (Greene & Cohen, 2004). Thus while decision-making

    1For a good review of the difculties in applying the insanity defense to defendants with frontal lobedysfunction see the work of Seiden (2004). The author discusses the emphasis the Virginia insanitydefense (which is similar to U.S. Supreme Court precedent and other state law) places on cognitive abilityand moral sense/reasoning, which is not impaired in frontal lobe patients, and the resulting challenge inapplying the defense to frontal lobe dysfunctional capital defendants. Similarly, an insanity defense is notthe best way to address questions of free will in the law, as this defense is (and should be) designed to carveout a very small population of defendants, whereas we have argued that the questions for free will are not soeasily limited.

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    Decision making and free will 275

  • research does give us cause to pull back on our legal systems notion that we operate

    with a will that is completely free, it is important to note that it has not addressed all

    the biological processes that are behind the conict between our retributive and our

    altruistic natures.

    What decision-making and other behavioral neuroscience research does allow us

    to do, however, is to appreciate this tension scientically. Guilt and innocence, fear

    and revenge are principles that by their nature arouse emotions that make it

    challenging for a society always to create the best solutions to the problems they fuel.

    Perhaps by providing us with some healthy distance from these emotions, a

    society-wide understanding of the neural mechanisms of will can contribute to a

    more popular appreciation of the complexity of the notion of responsibility. We have

    discussed the retribution justication rst because the new temperance in exacting

    retribution that neuroscience may inspire is important to keep in mind when

    considering some of the shortcomings of the other three justications.

    Deterrence

    The punitive systems goals of deterrence require that people be able to act on the

    prohibitions that the law denes, so an assumption of determinism may seem to

    render this a futile aim. However, decision-making research reveals more than just a

    disembodied mechanism of brain control. The mechanism we are discovering is one

    that in healthy individuals is inextricably linked to the stimuli that historically have

    existed in a persons environment, which would of course include laws, experiences

    of seeing the results of others violating laws or violating them oneself, and

    experiences of learning moral lessons about the activities that are the subjects of the

    laws. In other words, we are discovering one of the mechanisms by which deterrence

    operates, over the long term of an individuals neural development.

    On the other hand, we have seen in the cases of impaired will that, nonetheless,

    neurological conditions exist that result in people essentially ignoring experiences of

    punishment. That the cognitive prole of violent offenders is so similar to that of

    patients with just these conditions makes us wonder how, whether and to what

    degree punishment is working as a deterrent with any particular person. Perhaps the

    phenomenon of general deterrence (the deterrent effect that the possibility of

    punishment has for society) accounts for more of the concepts usefulness than does

    specic deterrence (the deterrent effect that being punished has on a particular

    offender). That is, in reforming our system, the biological foundations of the exercise

    of will may favor a forward-looking focus on how our justice system impacts the

    development of law-abiding behavioral patterns, over the more backward-looking,

    retributive focus that currently exists. This and similar hypotheses deserve further

    examination as decision-making research advances. The extremely high recidivism

    rates we experience in the US speak for themselves as evidence that imprisonment

    does not completely deter crime. In addition, the fact that criminal activity peaks in

    the late teens and early 20s, and drops off in the 30s and 40s for the vast majority of

    offenders, suggests the presence of additional deterrent factors that operate over

    time. These factors may be predominantly environmental (either natural, such as

    increased family responsibility, or imposed, as in punishments) or physiological (for

    example, maturation of the prefrontal cortex, which continues into the 20s). Our

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    276 K. Burns and A. Bechara

  • hope is that decision-making research will shed light on what are the most effective

    deterrents, and whether we can help their impact to be felt earlier in life.

    Incapacitation

    On the surface, the incapacitation justication is relatively unaffected by any

    research regarding choice and will. It is a practical justication: People who commit

    crimes need to be taken off of the streets, so that they are prevented from committing

    more crimes. The decision process that led to the crime is not explicitly relevant.

    However, the justication does rest to some degree on the assumption that there is a

    type of person who commits crimes, rather than a person who happens to have

    committed a crime, and so is also interrelated with the nal justication,

    rehabilitation.

    Rehabilitation

    Decision-making research is a double-edged sword in a conversation about

    rehabilitation. One the one hand, a deterministic view of the choice process seems to

    undermine the very idea of rehabilitation. On the other, the more we understand the

    brain, the greater our ability to design interventions that make the possibility of

    rehabilitation real for many whom the law writes off today. For example, research

    into the pharmacology of the different decision-making pathways indicates that the

    pathways that operate using non-conscious knowledge work using the neuro-

    transmitter dopamine, whereas conscious knowledge pathways make use of

    serotonin (Bechara, Damasio, & Damasio, 2001). This discovery raises the

    possibility of pharmacological interventions for individuals who suffer from chemical

    imbalances interfering with their ability to make adaptive choices. Of course,

    reversing the chemical deciency is not enough; therapy that enables the relearning

    of coping strategies in the presence of normal pharmacology is probably the most

    effective treatment. More research is necessary into clinical applications of the

    knowledge discussed in this article, which will create yet more rehabilitative

    opportunity.

    In discussing rehabilitative options, it is important to avoid pathologizing all

    things related to choice, conict and crime, a tendency that we nd in our society as

    psychological research advances in all areas. Moreover, discussion of rehabilitative

    therapies that are designed to effect how people exercise their will directly and

    alarmingly raises ethical questions including the following. Who is making the

    decision about what is a good exercise of will? Is the very notion of rehabilitation

    paternalistic? How much autonomy will society grant to offenders, especially violent

    offenders, in choosing not to submit to pharmacological or other intervention?

    Adequate discussion of these questions is outside the scope of this article, but should

    be foremost on our minds whenever we see the issues of free will and behavioral

    modications come together in any state-sponsored program. The issue of what to

    do when offenders either cannot or do not want to be rehabilitated remains despite

    what we learn from neuroscience, and should be considered in light of the

    understandings we have gained about the other justications for the criminal law

    system.

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    Decision making and free will 277

  • CONCLUSION

    Our exploration of the biology of human will and its implications for the legal system

    has highlighted the complexity of the interaction between the two. Like the other

    authors whose work we have cited, we are optimistic that society can embrace these

    and other discoveries in the behavioral and social sciences as an opportunity for

    creative reform rather than as a threat to our systems foundations. The law often

    changes slowly and conservatively, but we have already seen changes come in

    response to new understandings of human behavior, and expect that this pattern will

    only continue. Examples from the juvenile justice eld demonstrate how this

    evolution can work.

    The juvenile system has throughout its existence been dealing with precisely the

    questions that this article has been addressing about the extent to which our will is

    free versus the extent to which our environment and constitution determines our

    behavior. The separate juvenile system was in fact conceived with an understanding

    of the determined nature of the behavior of youth (Cotton, 2005), and has

    maintained this avor notwithstanding punitive changes that have been made in

    response to public fear of gang-involved youth. In recent years this characterization

    has been buoyed by greater understanding of the course of brain development, and

    the fact that even late in the teen years a persons judgment abilities are limited

    because the prefrontal cortex (exactly the area of the brain on which we have focused

    so much attention here) is not fully developed until the early 20s. This is not to say

    that the juvenile system is perfect; far from it: It suffers much from the unresolved

    issues of will and determinism, which affect whether we conceptualize the juvenile

    system as more criminal and punitive, or more civil and analogous to child welfare

    systems.2

    We do, however, see a greater willingness to innovate in the juvenile system, which

    likely is due to a corresponding willingness to release our retributive impulses,

    knowing what we do about youth psychology. For example, there is a movement

    toward introducing restorative justice models, based on the reconciliation

    commissions that have been successful in conict-torn regions, in our criminal

    justice system, which hasmade some progress in the youth justice eld. This model is

    reective, though perhaps unwittingly, of some of the brain science insights we

    proposed above for the justications of punishment. It is less harshly retributive,

    viewing offenses instead as occurring in a social and psychological context. It is more

    forward looking, as we suggested neurologically speaking might be a preferable way

    to inspire deterrence, and is open to more creative and collaborative notions of

    rehabilitation. Signicantly, the SupremeCourt also recently invalidated the juvenile

    death penalty (Roper v. Simmons, 2005), in response to changing societal notions of

    what are appropriate ways to deal with crime. These and other compassionate and

    creative possibilities exist for making our legal system compatible with the evolving

    denitions of responsibility, and better understandings of the neural mechanisms

    2See, for example,McKeiver v. Pennsylania (1971), a case in which the Supreme Court held that juvenilesdo not have the right to a trial by jury because of the differences between the juvenile and criminal system,reversing a trend toward granting juveniles in delinquency cases the constitutional protections affordedcriminal defendants.

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    278 K. Burns and A. Bechara

  • underlying choice will hopefully inspire greater openness to such innovations for

    juveniles as well as the adults they grow up to be.

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    Copyright # 2007 John Wiley & Sons, Ltd. Behav. Sci. Law 25: 263280 (2007)DOI: 10.1002/bsl

    280 K. Burns and A. Bechara

  • Figure

    1.Aschem

    aticdiagram

    illustratingkey

    structuresbelongingto

    theim

    pulsivesystem

    (red)andthereectivesystem

    (blue).Anem

    ergentdominantpatternof

    affectivesignalingcanmodulatetheactivityofseveralcomponentsoftheim

    pulsiveandreectivesystem

    s,whichincluderegionsinvolved

    in(1)representingpatternsof

    affectivestates,e.g.theinsulaandsomatosensingcortices,(2)triggeringofaffectivestates(e.g.amygdala(A)andVMPC),(3)mem

    ory,impulse,andattentioncontrol

    (e.g.lateralorbitofrontal,inferiorfrontalgyrus,dorsolateralprefrontal(D

    LPC),hippocampus(H

    yp),andanteriorcingulate

    (AC)),and(4)behavioralactions(e.g.

    striatumandsupplementarymotorarea).Wehaveproposedthatthemechanismsthatdeterminethevalence

    ofthedominantpatternofaffectivesignalingareconsistent

    withtheprinciplesofnaturalselection,i.e.survivalofthettest.In

    otherwords,numerousandconictingsignalsmaybetriggered

    simultaneously,butstrongeronesgain

    selectiveadvantageoverweakerones.Overthecourseofponderingadecision,positiveandnegativesignalsthatarestrongarereinforced,whileweakonesareeliminated.

    Thisprocesscanbeveryfast,andultim

    atelyawinner

    takes

    all,i.e.anoverall,more

    dominant,patternofaffectivesignalingem

    erges.

    Copyright # 2007 John Wiley & Sons, Ltd. Behav. Sci. Law 25: 263280 (2007)DOI: 10.1002/bsl