Department of Neurology, Division of Behavioral Neurology and Cognitive Neuroscience, University of Iowa College of Medicine, Iowa City, IA 52242, USA
![]() |
Abstract |
---|
![]() |
Introduction |
---|
The ventromedial sector includes both the gyrus rectus and mesial half of the orbital gyri, as well as the inferior half of the medial prefrontal surface, from its most caudal aspect to its most rostral in the frontal pole. Areas 11, 12, 13, 25, 32 and 10 of Brodmann are included in this sector, as is the white matter subjacent to all of these areas [see Fig. 1, areas marked in red; see also pp. 2425 of (Damasio, 1995
)]. Damage to the ventromedial sector disrupts social behavior profoundly. Previously well-adapted individuals become unable to observe social conventions and unable to decide advantageously on matters pertaining to their own lives. Remarkably, the patient's intellectual abilities are generally well preserved, in the sense that they have normal learning and memory, language and attention, and they even perform normally on many so-called executive function tests, such as the Wisconsin Card Sorting Test. Equally remarkably, these patients have an abnormality in their processes of emotion and feeling. The abnormality is such that they do not engage emotions in relation to complex situations and events, e.g. the emotion and ensuing feeling of embarrassment which are induced by specific social contexts (Damasio et al., 1991
; Damasio and Anderson, 1993
). The intriguing nature of these defects and the fact that they could not be accounted for by a primary problem with the availability of the pertinent social knowledge, with the ability to apply logic to such knowledge or with general defects of attention or language led to the development of an account known as the somatic marker hypothesis (Damasio, 1994
, 1996
).
|
![]() |
Background Assumptions |
---|
![]() |
Specifics of the Hypothesis |
---|
When subjects face a situation for which some factual aspects have been previously categorized, the pertinent dispositions are activated in higher-order association cortices. This leads to the recall of pertinently associated facts which are experienced in imagetic form. At the same time, the related ventromedial prefrontal linkages are also activated, and the emotional disposition apparatus is competently activated as well. The result of those combined actions is the reconstruction of a previously learned factualemotional set.
The re-activation described above can be carried out via a body loop, in which the soma actually changes in response to the activation and the ensuing changes are relayed to somatosensory cortices; or via an as-if body loop, in which the body is bypassed and re-activation signals are conveyed to the somatosensory structures which then adopt the appropriate pattern. From both evolutionary and ontogenetic perspectives, the body loop is the original mechanism but has been superseded by the as-if body loop and is possibly used less frequently than it. The results of either the body loop or the as-if body loop may become overt (conscious) or remain covert (non-conscious).
The establishment of a somatosensory pattern appropriate to the situation, via the body loop or via the as-if body loop, either overtly or covertly, is co-displayed with factual evocations pertinent to the situation and qualifies those factual evocations. This constrains the process of reasoning over multiple options and multiple future outcomes. For instance, when the somatosensory image which defines a certain emotional response is juxtaposed to the images which describe a related scenario of future outcome, and which triggered the emotional response via the ventromedial linkage, the somatosensory pattern marks the scenario as good or bad.
When this process is overt, the somatic state operates as an alarm or incentive signal. The somatic state is alerting you to the goodness or badness of a certain optionoutcome pair. The device produces its result at the openly cognitive level. When the process is covert the somatic state constitutes a biasing signal. Using a non-conscious influence, e.g. through a non-specific neurotransmitter system, the device influences cognitive processing.
Certain optionoutcome pairs can be rapidly rejected or endorsed, and pertinent facts can be more effectively processed. The hypothesis thus suggests that somatic markers normally help constrain the decision-making space by making that space manageable for logic-based, costbenefit analyses. In situations in which there is remarkable uncertainty about the future and in which the decision should be influenced by previous individual experience, such constraints permit the organism to decide efficiently within short time intervals.
In this article we review a number of findings related to the investigation of the somatic marker hypothesis in human subjects with ventromedial prefrontal cortex (VM) damage. The lesions of some of the subjects who participated in the experiments described below are presented in Figure 1.
![]() |
The Role of the VM in Decision Making |
---|
The study of the decision-making impairment of patients with VM lesions required an instrument for the detection and measurement of such impairments in the laboratory. The development of a card task known as the gambling task (Bechara et al., 1994) provided this tool. The essential feature of this task is that it mimics real-life situations in the way it factors uncertainty, reward and punishment. The task involves four decks of cards, named A, B, C and D. The goal is to maximize profit on a loan of play money. Subjects are required to make a series of 100 card selections, but are not told ahead of time how many card selections they are going to be allowed to make. Cards can be selected one at a time, from any deck, and subjects are free to switch from any deck to another, at any time and as often as they wish. The decision to select from one deck or another is largely influenced by schedules of reward and punishment. These schedules are pre-programmed and known to the examiner, but not to the subject (Bechara et al., 1994
, 1999a
). They are arranged in such a way that every time the subject selects a card from deck A or B, s/he gets $100, and every time deck C or D is selected, the subject gets $50. However, in each of the four decks, subjects encounter unpredictable money loss (punishment). The punishment is set to be higher in the high-paying decks A and B, and lower in the low-paying decks C and D. In decks A and B the subject encounters a total loss of $1250 in every 10 cards. In decks C and D the subject encounters a total loss of $250 in every 10 cards. In the long term, decks A and B are disadvantageous because they cost more, a loss of $250 in every 10 cards. Decks C and D are advantageous because they result in an overall gain in the end, a gain of $250 in every 10 cards.
Insensitivity to Future Consequences following Bilateral Damage of the Prefrontal Cortex
A large sample of normal control subjects (n = 82, balanced in terms of gender, with 820 years of education, and between the ages of 20 and 64) has been tested with the original card version of the gambling task described above. Patients with lesions in different sectors of the frontal lobe (n = 45), or with lesions in areas of the lateral temporal cortex or occipital cortex (n = 35) have also been tested. Since the original manual version of the gambling task was described, a new computer version has been devised, and similar numbers of control subjects and patients have been tested with the new computer version. The results from either version of the gambling task are interchangeable. As the task progresses from the first to the 100th trial, normal controls gradually make more selections of cards from the good decks (C and D) and less selections from the bad decks (A and B) (Fig. 2 left). Patients with lesions in the dorsolateral sector of the prefrontal cortex (Bechara et al., 1998
), or in areas outside the prefrontal cortex (Bechara et al., 1994
), perform in a manner similar to that of normal subjects. In sharp contrast, patients with bilateral lesions of the VM do not increase the number of their selection of cards from the good decks (C and D); they persist in selecting more cards from the bad decks (A and B) (Fig. 2
left). The card selection profiles from normal controls show that a typical normal subject initially samples all decks and repeats selections from the bad decks A and B, probably because they pay more. However, eventually the normal subject switches to more and more selections from the good decks C and D, with only occasional returns to decks A and B. On the other hand, a typical VM patient behaves like a normal subject only in the first few selections. The patient begins by sampling all decks and selecting from decks A and B, and then makes several selections from decks C and D, but then soon returns more and more to decks A and B (Fig. 2
right).
|
In the VM patient population, the decision-making impairment, as measured by the gambling task, is stable over time. When a sample of six VM frontal patients and five normal controls were re-tested after various time intervals (1 month after the first test, 24 h later and for the fourth time, 6 months later), the performance of VM patients did not improve. On the other hand, the performance of normal controls improved significantly over time (Fig. 3).
|
Biases Guide Decisions
The results described above prompted the following question: what is the basis for the myopia for the future that plagues VM frontal patients? For many years, many theorists of decision making assumed that the feelings triggered when making a decision or a risky choice were not integral to the decision-making process. In this sense, the decision-making theorists assumed that risky decision making was essentially a cognitive activity devoid of an emotional component. These theories suggest that people assess the possible outcomes of their actions through some type of costbenefit analysis. However, several authors have proposed an alternative theoretical account which highlights the role of the affect experienced during the time of deliberation prior to making decisions (Schwartz and Clore, 1983; Zajonc, 1984
; Damasio et al., 1990
).
Evidence in support of this idea comes from studies of normal control subjects and patients with bilateral VM frontal damage during their performance on the gambling task, and the analysis of their psychophysiological activity during task performance (Bechara et al., 1996). Skin conductance response (SCR) activity has been recorded so far in a large sample of normal subjects (n = 55) and VM patients (n = 15) during the performance of the gambling task. Despite some variations in the methods for collecting the SCR data (Bechara et al., 1996
, 1999a
), the general principles remain the same. Every time the subject picks a card, the deck from which that card was picked is recorded, and the magnitude of the SCR in the time window (~5 s) right before the subject picked the card is measured. In addition, the magnitude of the SCR in the time window (~5 s) after the card was picked is also measured. Thus, three types of responses are identified. (i) The reward SCRs, those occurring after turning cards with reward only. (ii) The punishment SCRs, those occurring after turning cards with reward and punishment. (iii) The anticipatory SCRs, those occurring before turning a card from a deck, during the time the subject ponders from which deck to choose (Bechara et al., 1996
).
The results from the psychophysiological experiments conducted so far reveal that normal controls and VM patients generate SCRs as a reaction to reward or punishment. Normal controls, however, as they become experienced with the task, also begin to generate SCRs before the selection of any card. The anticipatory SCRs generated by normal controls: (i) develop over time (i.e. after selecting several cards from each deck, and thus encountering several instances of reward and punishment); and (ii) actually become more pronounced before selecting cards from the disadvantageous decks (A and B). These anticipatory SCRs are absent in the VM patients (Fig. 4). This suggests that VM patients have a specific impairment in their ability to generate anticipatory SCRs in response to a possible outcome of their action. Since SCRs are physiological indices of an autonomically controlled change in somatic state, it seems reasonable to conclude that the absence of anticipatory SCRs is an indication that these patients' ability to change somatic states in response to an imagined scenario is severely compromised. In this perspective, the failure to enact a somatic state appropriate to the consequences of a response would be a correlate of their inability to choose advantageously.
|
None of the bilateral VM patients tested so far have performed advantageously on the gambling task. However, not every normal control subject performs advantageously. Approximately 20% of normal adults who describe themselves as high-risk takers in real life end up selecting more cards from the bad decks relative to the good ones (Bechara et al., 1999a). When looking at the anticipatory SCRs in these normal individuals, it is often found that the magnitudes of the anticipatory SCRs in relation to the bad decks are slightly lower than those in relation to the good decks (Bechara et al., 1999a
). The opposite is true (i.e. higher anticipatory SCRs with the bad decks relative to the good decks) in normal individuals who play advantageously. The most critical distinction between these normal individuals and the VM patients, however, is that these normal individuals do generate anticipatory SCRs. The VM patients, on the other hand, do not generate anticipatory SCRs at all. These physiological results are very important because they separate individuals with high-risk-taking behavior from individuals with VM frontal lobe dysfunction. When taking a risk, the somatic states signaling the possible negative consequences of the outcome are enacted. However, the individual can override these biases by higher cognitive processes. In the case of VM damage, these biases are never enacted and never enter the decision-making process. This suggests that taking a risk is not the same as having poor judgement and impaired decision making. The issue of risk taking versus decision making was addressed in a previous study that showed that orbitofrontal patients risked significantly less of their accumulated reward than controls, thus suggesting a pattern of conservative behavior (Rogers et al., 1999
). Yet, these same patients made suboptimal choices and spent more time deliberating their choices (Rogers et al., 1999
). Another study suggested that while frontal patients were impulsive and made poor decisions, they did not express a high-risk-taking behavior (Miller, 1992
). This evidence suggests that risk-taking behavior and impaired decision making are not synonymous.
Biases Do Not Need To Be Conscious
Given the important role that biases play in decision making, it is important to determine if these anticipatory responses (biases) develop after the subject knows which decks are good or bad, or if they precede such explicit knowledge. This question was addressed in an experiment in which ten normal subjects and six VM frontal patients were tested on the gambling task, while their SCRs were being recorded as before. However, in this experiment, every time a subject had picked ten cards the game was stopped briefly and the subject was asked to describe whatever s/he knew was going on in the game (Bechara et al., 1997). The analysis of the subjects' answers suggested that they went through four distinct periods across the task. The first was a pre-punishment period, when subjects sampled the decks, before they encountered any punishment. The second was a pre-hunch period, when subjects began to encounter punishment, but had no clue about what was going on in the game. The third was a hunch period, when subjects began to express a hunch about the decks that were riskier, even if they were not sure about their guess. The fourth was a conceptual period, when subjects knew very well the contingencies in the task, which decks were the good ones, which decks were the bad ones and why this was so (Fig. 5
). It is interesting that 30% of the control subjects did not reach the fourth, or conceptual, period in this experiment, yet they performed normally on the gambling task.
|
These results show that VM frontal patients continue to choose disadvantageously in the gambling task, even after realizing the consequences of their action. This suggests that the anticipatory SCRs represent unconscious biases, probably derived from prior experiences with reward and punishment. These biases help deter the normal subject from pursuing a course of action that is disadvantageous in the future. This biasing effect occurs even before the subject becomes aware of the goodness or badness of the choice s/he is about to make. Even without these biases, the knowledge of what is right and what is wrong may become available, as happened in 50% of the VM patients. However, by itself, such knowledge is not sufficient to ensure an advantageous behavior. Although the frontal patient may be fully aware of what is right and what is wrong, s/he still fails to act accordingly. These patients may say the right thing, but do the wrong thing.
![]() |
Relationship between Emotion, Memory and Decision Making |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Decision Making and Working Memory are Distinct Operations of the Prefrontal Cortex
The rationale for the notion that working memory and decision making are distinct functions comes from the observations that VM frontal patients suffer from impairments in decision making, while preserving a normal level of memory and intellect. On the other hand, although some DL frontal patients complain of memory impairments, they do not appear to suffer from impairments in decision making, as judged from their behavior in real life. Using modified delay-task procedures (delayed response and delayed non-matching to sample) to measure working memory (Goldman-Rakic, 1987; Fuster, 1991
), and the gambling task to measure decision making, the following experiment was performed. A group of 21 normal control subjects, nine patients with bilateral VM frontal lesions and ten patients with right or left lesions of the DL sector of the prefrontal cortex were tested on the delay and gambling tasks (Bechara et al., 1998
). The gambling task was the same task mentioned previously, and the delay task procedures were modifications of classical delay tasks.
Delay tasks that are used in non-human primates are too simple for use with humans. Therefore, a distracter was introduced during the delay between the cue and the response. The purpose of the distracter was to interfere with the ability of the subject to rehearse the position or the color of the cues during the delay, and thus to increase the demands of the tasks on working memory. In the delayed response experiment, four cards appeared for 2 s on a computer screen, with two of the cards face down and the other two face up, showing red or black colors. The cards disappeared for one, 10, 30 or 60 s and then reappeared, but this time all the cards were face down. The correct response was to select the two cards that were initially face up. During the delay, the subject had to read aloud a series of semantically meaningless sentences. Scores were calculated as the percent of correct choices made by the subject at the 10, 30 and 60 s delays. Impaired performance on the delayed response task was defined as achieving a percent correct score of 80 or less at the 60 s delay, a cutoff score below which no normal control ever performed (Bechara et al., 1998). In the delayed non-matching to sample experiment, the task was similar to the delayed response task except that only one card appeared initially on the computer screen for 2 s. The card was face up and was either red or black. After the card disappeared for 1, 10, 30 or 60 s, four cards appeared on the screen, all face up, two of which were red and two black. The correct response was to select the two cards that were opposite in color (non-matching) to the initial sample card.
In this experiment we used two types of delay tasks because studies in non-human primates show that different areas of the DL frontal cortex are associated with different domains of working memory. The inferior areas of the dorsolateral sector have been associated with object memory, whereas the superior areas have been associated with spatial memory (Goldman-Rakic, 1987, 1992
; Wilson et al., 1993
). Similar dissociations were found in humans (Courtney et al., 1996
). The delayed response tasks have been designed to tax the spatial (where) domain of working memory, whereas the delayed non-matching to sample tasks are supposed to tax the object (what) domain of working memory (Fuster, 1990
; Wilson et al., 1993
). Since the lesions in the patients we studied were not restricted to the inferior or superior regions, and the lesions spanned a wide area of DL frontal cortices, we used both types of delayed tasks because we anticipated that both domains of working memory (spatial and object) may be affected. In other words, our attempt was not to sort out differences between different types of working memory, but rather to cover a range of working memory with one task. Therefore, the results we report here are an average of the results obtained from both delay tasks. In the next section, we use the term delay tasks' to refer to both procedures (delayed response and delayed non-matching to sample) [results obtained with each individual delay task are given elsewhere (Bechara et al., 1998
)].
This experiment revealed two intriguing findings. First, working memory is not dependent on the intactness of decision making, i.e. subjects can have normal working memory in the presence or absence of deficits in decision making. Some VM frontal patients who were severely impaired in decision making (i.e. abnormal in the gambling task) had superior working memory (i.e. normal in the delay tasks). On the other hand, decision making seems to be influenced by the intactness or impairment of working memory, i.e. decision making is worse in the presence of abnormal working memory. Patients with right DL frontal lesions and severe working memory impairments showed low normal results in the gambling task (Fig. 6). In summary, working memory and decision making were asymmetrically dependent. Second, although all VM patients tested in this experiment were impaired on the gambling task, they were split in their performance in the delay tasks. Five patients were abnormal in the delay tasks (Abnormal Gambling/Abnormal Delay) and four were normal in the delay tasks (Abnormal Gambling/Normal Delay) (Fig. 7, graphs
). The most important finding is that all patients in the Abnormal Gambling/Abnormal Delay group had lesions that extended posteriorly, possibly involving the basal forebrain region. However, the other group (Abnormal Gambling/Normal Delay) had lesions that were more anterior and did not involve the basal forebrain (Fig. 7, anatomy
).
|
|
|
These findings reveal a double dissociation (cognitive and anatomic) between deficits in decision making (anterior VM) and working memory (right DL). They reinforce the special importance of the VM region in decision making, independently of a direct role in working memory.
The Emotional Mechanism that Biases Decision Making is Distinct from the Emotional Mechanism that Improves Memory
The previous discussion leads to the question of whether the mechanism by which emotion improves memory is the same as, or different from, the mechanism through which emotion biases decisions. The amygdala has been found to be necessary for emotions to improve memory (Cahill et al., 1995). Our own work has also shown that the amygdala is important in the creation of biases and in decision making (Bechara et al., 1999a
). This suggests that in the amygdala, the mechanisms through which emotion modulates memory and decision making may be inseparable. The remaining question is whether these mechanisms might be separable in the VM cortex. In order to answer this last question, we tested 12 normal control subjects and six VM patients with anterior lesions that spared the basal forebrain for their memory of a series of neutral and emotionally charged pictures. The series of pictures involved four sets, with four pictures in each set. Each set of four pictures contained two neutral (e.g. farm scenes) and two emotional (e.g. raped and mutilated bodies') pictures. The pictures in set 1 were presented once each; those in set 2 were presented twice each; in set 3, four times each; and in set 4, eight times each. Five minutes after viewing all the pictures, subjects were tested for their recall of each picture they saw, and for the overall content of the picture. The recall of picture content was calculated for each subject as a function of repetition times and emotional content.
As might be expected, both normal controls and VM patients showed improved memory as a result of repetition. The most important finding, however, was that both groups showed a response to the emotion manipulation, producing a better memory curve for pictures with emotional content than for neutral pictures (Fig. 8). Thus, this experiment actually separated the memory curve that is a function of repetition from the curve that is a function of emotional content. The results indicate that the VM patients are able to use emotional content in order to enhance their memory, suggesting that the mechanism through which emotion modulates decision making is different from that through which emotion modulates memory. These results also support the conclusion that the decision-making impairment of VM patients cannot be explained by a deficit in the recall of emotional events.
|
![]() |
Why Do VM Frontal Patients Fail to Trigger Somatic States when They Contemplate Decisions? |
---|
Emotional Conditioning
We have tested whether one reason for VM frontal patients to fail to trigger anticipatory biases (anticipatory SCRs) when contemplating a decision in the gambling task is due to a failure to couple an exteroceptive stimulus (or event) with the somatic state of a punishment. These patients may have a defect in acquiring fear conditioning. To test this possibility directly, we used a fear-conditioning procedure, which consisted of using four different colors of monochrome slides as conditioned stimuli (CS) and a startlingly aversive loud sound (100 db) as the unconditioned stimulus (US) (Bechara et al., 1995). Electrodermal activity (SCR) served as the dependent measure of autonomic conditioning. The emotional conditioning of each subject included three phases: (i) a habituation phase; (ii) a conditioning phase. In this phase, only one of the colors was paired with the US. These CS slides were presented at random among the other colors; and (iii) an extinction phase.
A group of ten VM patients and ten matched control subjects were tested in the experiment just mentioned. The VM patients did condition to the loud noise (Tranel et al., 1996; Bechara et al., 1999a
). This suggests that the VM cortex is not essential for emotional conditioning. Consequently, it is reasonable to assume that the failure of VM patients to acquire anticipatory SCRs in the gambling task, and their decision-making impairment, cannot be explained by a failure to acquire conditioned emotional responses.
The Experience of Emotions
Recently, we have started to address the question of whether one reason that VM frontal patients fail to trigger anticipatory biases (anticipatory SCRs) is the inability to re-experience the emotional state associated with punishment when recalling previous instances of punishment. A variety of procedures can be used to induce emotions in human subjects, such as watching emotional film clips, looking at pictures charged with emotions or recalling highly emotional personal events. In this preliminary study, emotional imagery was used as a method to induce emotional states. The subjects are asked to think about and describe a situation in their lives in which they felt each of the following emotions: happiness, sadness, fear and anger. After a brief description of each story is obtained, the subject is asked to imagine and re-experience each emotional situation while their physiological activity (SCR, heart rate, respiratory frequency, skin temperature and facial EMG) is monitored. As a control condition, the subject is also asked to recall and imagine a nonemotional situation, e.g. getting up that morning, showering, dressing up, having breakfast and then going to work.
We tested eight VM patients with this procedure. They were all able to retrieve previous emotional experiences. Most importantly, they generated higher physiological activity (e.g. SCR and heart rate) during the imagery of the angry situations than during the neutral situations (Damasio et al., 1997; Tranel et al., 1998
). Although all the VM patients reliably re-experienced anger, the re-experience of fear was less reliable, i.e. some could not experience it at all, and those who could did so with a less intense response. Whereas the VM patients were able to reexperience anger and in some cases fear, most of them had difficulties conjuring up a happy or sad emotion. This suggests that damage to the VM cortex weakens the ability to re-experience an emotion from the recall of an appropriate emotional event. Consequently, it is reasonable to assume that the failure of VM patients to acquire anticipatory SCRs, coupled to their decision-making impairment, is in part due to their inability to re-experience the emotion of a previously fearful situation. Obviously, this is a preliminary finding that requires further investigation.
The same is also true for the induction of an emotion by external stimuli such as the viewing of emotionally charged pictures. Indeed, earlier studies showed that VM patients failed to generate SCRs to emotionally charged pictures when they viewed these pictures passively (Damasio et al., 1990). However, the same patients generated normal magnitude SCRs to the same target pictures when they were asked to view and describe the content of the pictures (Damasio et al., 1990
). During the gambling task, VM patients would generate SCRs when they lost a large sum of money, but the magnitude of these SCRs was never as high as that of normal controls (Bechara et al., 1999a
). Together, these results suggest that these patients may have a weakened ability to process the affective attribute of an emotional stimulus or to actually experience the emotion associated with that stimulus. This weakness may contribute to the failure to trigger somatic states when deliberating about options for a decision. However, the fact that these VM patients are not completely emotionless suggests that this weakness is not the sole factor responsible for the failure. Nonetheless, it is an intriguing thought that if the experience of punishment would be more intense, the VM patients might overcome the failure to re-experience the emotional state of punishment, and therefore improve the decision-making impairment. For instance, in the gambling task, if the punishment was made several times the amount that is effective in normal subjects, it may become effective and VM patients might begin to choose advantageously.
![]() |
The Issue of Impulsiveness and Response Inhibition |
---|
First, it is important to distinguish between motor and cognitive impulsiveness. Motor impulsiveness is usually studied in animals under the umbrella of response inhibition. After establishing a habit to respond to a stimulus that predicts a reward, there is a sudden change in the contingencies of the task that requires the inhibition of the previously rewarded response. Go/no-go tasks, delayed alternation and response shifting are examples of experimental design that measure this type of impulsive behavior (Mishkin, 1964; Freedman, 1986
; Diamond, 1990
; Fuster, 1990
; Stuss, 1992
; Dias et al., 1996
; Freedman et al., 1998
). In humans, impulsive behavior is often uncovered in neuropsychological tasks that detect perseverative errors, such as the Wisconsin Card Sorting Task, or in experimental tasks such as delayed alternation (Freedman, 1986
; Freedman et al., 1998
). Cognitive impulsiveness, on the other hand, which can be seen as related to an inability to delay gratification, is a more complex form of disinhibited behavior. Cognitive impulsiveness may be illustrated with the example in which a child sees a piece of a candy on the table and is told by the parent no, you must wait 30 min before you can have the candy; otherwise, you face punishment. The child understands the information and holds for a short while but after 2 min can no longer delay the gratification, resist the temptation and inhibit the response to reach for the candy.
Previous studies have shown that VM patients with lesions that spare the basal forebrain do not show motor impulsiveness and do not perseverate in conventional neuropsychological tests, although those with lesions that involve the basal forebrain may (Bechara et al., 1998). We can also state that VM patients during their performance of the gambling task switch decks whenever they receive punishment, just as normal controls do. Such a performance does not suggest a lack of inhibition to a previously rewarding response (Fig. 2
). VM patients are also unimpaired in delay task procedures (i.e. delayed non-matching to sample) considered sensitive to deficits in response inhibition (Bechara et al., 1998
).
On the other hand, the behavior of VM patients in the gambling task, and in real life, can be viewed as similar to the cognitive impulsiveness of the child with the candy. That is to say, when the patients are presented with a deck of cards which yields a large immediate reward, even if it can cost a large loss in the future, the patients seem unable to delay the gratification of the reward for too long. Their tendency to return quickly and more often to the decks that yield high immediate reward seems to suggest such a mechanism. The question, however, is who decides when to suppress, or not to suppress, such a response as the seeking of a large immediate reward? Somatic states may indeed serve as the decision maker in such a situation. The following is a proposal of how somatic states may interact with mechanisms of response inhibition.
Using the impulsive behavior of the child with the candy as an illustrative example, one can see the conflict created by the decision to reach or not to reach for the candy. There are positive somatic states generated by the immediate and available reward (the candy), or the large sum of money in the gambling task. On the other hand, there are negative somatic states generated by the delayed punishment threatened by the parent or the possible loss of a large sum of money in the gambling task. If the threat of punishment were severe enough, then the evoked negative somatic states generated by that threat would counteract the positive somatic states produced by the immediate reward. The choice to seek the reward would thus be marked with a negative value, and the response to reach for the immediate reward might be inhibited. However, if the situation were that of a mild punishment, which would let the immediate reward outweigh the future punishment, the negative somatic states triggered by the possible punishment might not be sufficiently strong to counteract the positive states triggered by the immediate reward. In this case, the choice would be marked with a positive value. In our example, the child reaches for the candy and the behavior may be considered normal, advantageous and not impulsive. This example illustrates two different readings of the same situation involving an immediate reward and a future punishment. The difference, however, is that in one situation the inhibition of the action to seek the reward should be inhibited because the delayed punishment outweighs the immediate reward. In the other situation, the action to seek the reward should not be inhibited because the immediate reward outweighs the delayed punishment. The construct of impulsiveness and response inhibition by itself does not explain when to inhibit a given response or not. The activation of somatic states provides the important signals leading to whether to inhibit the response under consideration or not.
![]() |
Conclusion |
---|
The somatic marker hypothesis and the experimental strategies used to study decision making in neurological patients provide parallels and direct implications for understanding the nature of several psychiatric disorders. For instance, substance abusers are similar to VM patients in that when faced with a choice that brings some immediate reward (i.e. taking a drug), at the risk of incurring a loss of reputation, job, home and family, they choose the immediate reward and ignore the future consequences. Using the gambling task (Grant et al., 1997; Petry et al., 1998
; Bechara et al., 1999b
) or related decision-making tasks (Rogers et al., 1999
), recent studies have indicated that impairment in decision making may stand at the core of the problem of substance abuse. Similarly, the personality profile of VM patients bears some striking similarities to psychopathic (or sociopathic) personality, so much so that we have used the term acquired sociopathy to describe the condition of patients with VM damage (Damasio et al., 1990
). The qualifier acquired signifies that the condition in VM patients follows the onset of brain injury, and occurs in persons whose personalities and social conduct were previously normal. The patients are usually not destructive or harmful to others, a feature that tends to distinguish the acquired form of the disorder from the standard developmental form. Indeed, recent evidence has indicated that the earlier the onset of VM damage, the more severe the antisocial behavior, suggesting that early dysfunction in the prefrontal cortex may, by itself, cause abnormal development of social and moral behavior (Anderson et al., 1999
). Recent studies have begun to look at the possibility that the psychopathic behavior seen in cases in which no neurological history has been identified may be linked to abnormal operation of the neural system involving the VM (Schmitt et al., 1999
). Finally, in addition to the disorders mentioned above, applications of the somatic marker hypothesis may extend to psychiatric disorders that include schizophrenia (Wilder et al., 1998
), pathological gambling, depression, and attention deficit and hyperactivity disorders (ADHD).
![]() |
Notes |
---|
Address correspondence to Antonio R. Damasio, Department of Neurology, University of Iowa Hospitals and Clinics, Iowa City, IA 52242, USA. Email: antonio-damasio{at}uiowa.edu (damasio{at}mail.medicine.uiowa.edu).
![]() |
References |
---|
Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50:715.[ISI][Medline]
Bechara A, Tranel D, Damasio H, Adolphs R, Rockland C, Damasio AR (1995) Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science 269: 11151118.[ISI][Medline]
Bechara A, Tranel D, Damasio H, Damasio AR (1996) Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. Cereb Cortex 6:215225.[Abstract]
Bechara A, Damasio H, Tranel D, Damasio AR (1997) Deciding advantageously before knowing the advantageous strategy. Science 275:12931295.
Bechara A, Damasio H, Tranel D, Anderson SW (1998) Dissociation of working memory from decision making within the human prefrontal cortex. J Neurosci 18:428437.
Bechara A, Damasio H, Damasio AR, Lee GP (1999a) Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 19:54735481.
Bechara A, Dolan S, Hindes A, Anderson SW, Nathan P (1999b) Decision-making deficits, linked to a dysfunctional orbitofrontal cortex, revealed in alcohol and stimulant abusers. Soc Neurosci Abstr (in press).
Cahill L, Babinsky R, Markowitsch HJ, McGaugh JL (1995) The amygdala and emotional memory. Nature 377:295296.[ISI][Medline]
Courtney SM, Ungerleider LG, Keil K, Haxby JV (1996) Object and spatial visual working memory activate separate neural systems in human cortex. Cereb Cortex 6:3949.[Abstract]
Courtney SM, Ungerleider LG, Keil K, Haxby JV (1997) Transient and sustained activity in a distributed neural system for human working memory. Nature 386:608611.[ISI][Medline]
Damasio AR (1989a) The brain binds entities and events by multiregional activation from convergence zones. Neural Computat 1:123132.
Damasio AR (1989b) Time-locked multiregional retroactivation: a systems-level proposal for the neural substrates of recall and recognition. Cognition 33:2562.[ISI][Medline]
Damasio AR (1994) Descartes' error: emotion, reason, and the human brain. New York: Grosset/Putnam.
Damasio H (1995) Human brain anatomy in computerized images. New York: Oxford University Press.
Damasio AR (1996) The somatic marker hypothesis and the possible functions of the prefrontal cortex. Phil Trans R Soc Lond B 351: 14131420.[ISI][Medline]
Damasio AR, Anderson SW (1993) The frontal lobes. In: Clinical neuropsychology (Heilman KM, Valenstein E, eds), pp. 409460. New York: Oxford University Press.
Damasio AR, Damasio H (1994) Cortical systems for retrieval of concrete knowledge: the convergence zone framework. In: Large scale neuronal theories of the brain (Koch C, ed.), pp. 6174. Cambridge, MA: MIT Press.
Damasio AR, Tranel D, Damasio H (1990) Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli. Behav Brain Res 41:8194.[ISI][Medline]
Damasio AR, Tranel D, Damasio H (1991) Somatic markers and the guidance of behavior: theory and preliminary testing. In: Frontal lobe function and dysfunction (Levin HS, Eisenberg HM, Benton AL, eds), pp. 217229. New York: Oxford University Press.
Damasio H, Bechara A, Tranel D, Damasio AR (1997) Double dissociation of emotional conditioning and emotional imagery relative to the amygdala and right somatosensory cortex. Soc Neurosci Abstr 23: 1318.
Denburg NL, Bechara A, Tranel D, Hindes AR, Damasio AR (1999) Neuropsychological evidence for why the ability to decide advantageously weakens with advancing age. Soc Neurosci Abstr 25:32.
D'Esposito M, Detre JA, Alsop DC, Shin RK, Atlas S, Grossman M (1995a) The neural basis of central execution systems of working memory. Nature 378:279281.[ISI][Medline]
D'Esposito M, Shin RK, Detre JA, Incledon S, Annis D, Aguirre GK, Grossman M, Alsop DC (1995b) Object and spatial working memory activates dorsolateral prefrontal cortex: a functional MRI study. Soc Neurosci Abstr 21:1498.
Diamond A (1990) The development and neural bases of higher cognitive functions. New York: New York Academy of Sciences.
Dias R, Robbins TW, Roberts AC (1996) Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380:6972.[ISI][Medline]
Easterbrook JA (1959) The effect of emotion on cue utilization and the organization of behavior. Psychol Rev 66:183201.[ISI]
Freedman M (1986) Bilateral frontal lobe disease and selective delayed response deficits in humans. Behav Neurosci 100:337342.[ISI][Medline]
Freedman M, Black S, Ebert P, Binns M (1998) Orbitofrontal function, object alternation and perseveration. Cereb Cortex 8:1827.[Abstract]
Fuster JM (1990) Prefrontal cortex and the bridging of temporal gaps in the perceptionaction cycle. In: The development and neural bases of higher cognitive functions. (Diamond A, ed.), pp. 318336. New York: Annals of the New York Academy of Science.
Fuster JM (1991) The prefrontal cortex and its relation to behavior. In: Progress in brain research (Holstege G, ed.), pp. 201211. New York: Elsevier Science Publishers.
Fuster JM (1996) The prefrontal cortex. Anatomy, physiology, and neuropsychology of the frontal lobe. New York: Raven Press.
Goldman-Rakic PS (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. In: Handbook of physiology; the nervous system (Plum F, ed.), pp. 373401. Bethesda, MD: American Physiological Society.
Goldman-Rakic PS (1992) Working memory and the mind. Scient Am 267:111117.
Grant S, Contoreggi C, London ED (1997) Drug abusers show impaired performance on a test of orbitofrontal function. Soc Neurosci Abstr 23:1943.
Janis IL, Mann L (1977) Decision-making: a psychological analysis of conflict, choice, and commitment. New York: Free Press.
Jonides J, Smith EE, Koeppe RA, Awh E, Minoshima S, Mintun MA (1993) Spatial working memory in humans as revealed by PET. Nature 363:623625.[ISI][Medline]
LeDoux J (1996) The emotional brain: the mysterious underpinnings of emotional life. New York: Simon and Schuster.
LeLand DS, Richardson JS, Vankov A, Grant SJ, Pineda JA (1998) Decision-making and associated ERPS in low-and high-dependence smokers performing the Iowa gambling task. Soc Neurosci Abstr 24:1175.
Mann L (1992) Stress, affect, and risk taking. In: Risk-taking behavior (Frank YJ, ed.), pp. 202230. Chichester: Johm Wiley & Sons.
McCarthy G, Blamire AM, Puce A, Nobre AC, Boch G, Hyder F, Goldman-Rakic P, Shulman RG (1994) Functional magnetic resonance imaging of human prefrontal cortex activation during a spatial working memory task. Proc Natl Acad Sci USA 91:86908694.[Abstract]
Miller LA (1992) Impulsivity, risk-taking, and the ability to synthesize fragmented information after frontal lobectomy. Neuropsychologia 30:6979.[ISI][Medline]
Milner B, Petrides M, Smith ML (1985) Frontal lobes and the temporal organization of memory. Hum Neurobiol 4:137142.[ISI][Medline]
Mishkin M (1964) Perseveration of central sets after frontal lesions in monkeys. In: The frontal granular cortex and behavior (Akert JM, Wa K, eds), pp. 219241. New York: McGraw-Hill.
Petrides M (1996) Specialized systems for the processing of mnemonic information within the primate frontal cortex. Phil Trans R Soc Lond 351:14451457.[ISI][Medline]
Petrides M, Alivisatos B, Meyer E, Evans AC (1993) Functional activation of the human frontal cortex during the performance of verbal working memory tasks. Proc Natl Acad Sci USA 90:878882.[Abstract]
Petry NM, Bickel WK, Arnett M (1998) Shortened time horizons and insensitivity to future consequences in heroin addicts. Addiction 93:729738.[ISI][Medline]
Reavis R, Overman WH, Hendrix S, Exposito W, Dezio-Cottle C (1998) Possible double dissociation of function between adult males and females in two brain system. Soc Neurosci Abstr 24:1177.
Rogers RD, Everitt BJ, Baldacchino A, Blackshaw AJ, Swainson R, Wynne K, Baker NB, Hunter J, Carthy T, Booker E, London M, Deakin JFW, Sahakian BJ, Robbins TW (1999) Dissociable deficits in the decision-making cognition of chronic amphetamine abusers, opiate abusers, patients with focal damage to prefrontal cortex, and tryptophan-depleted normal volunteers: evidence for monoaminergic mechanisms. Neuropsychopharmacology 20:322339.[ISI][Medline]
Rolls ET (1999) The brain and emotion. Oxford: Oxford University Press.
Roozendaal B, Cahill L, McGaugh JL (1996) Interaction of emotionally activated neuromodulatory systems in regulating memory storage. In: Brain processes and memory (Ishikawa K, McGaugh JL, Sakata H, eds), pp. 3954. Amsterdam: Elsevier.
Schmitt WA, Brinkley CA, Newman JP (1999) Testing Damasio's somatic marker hypothesis with psychopathic individuals: risk-takers or risk-averse? J Abnorm Psychol (in press).
Schwartz N, Clore GL (1983) Mood, misattribution, and judgements of well-being: information and directive functions of affective states. J Person Soc Psychol 45:513523.
Shallice T (1993) From neuropsychology to mental structure. Cambridge: Cambridge University Press.
Smith EE, Jonides J, Koeppe RA, Awh E, Schumacher EH, Minoshima S (1995) Spatial versus object working memory: PET investigations. J Cogn Neurosci 7:337356.[ISI]
Stuss DT (1992) Biological and psychological development of executive functions. Brain Cogn 20:823.[ISI][Medline]
Swartz BE, Halgren E, Fuster JM, Simpkins F, Gee M, Mandelkern M (1995) Cortical metabolic activation in humans during a visual memory task. Cereb Cortex 3:205214.
Tranel D, Bechara A, Damasio H, Damasio AR (1996) Fear conditioning after ventromedial frontal lobe damage in humans. Soc Neurosci Abstr 22:1108.
Tranel D, Bechara A, Damasio H, Damasio AR (1998) Neural correlates of emotional imagery. Int J Psychophys 30:107.
Wilder KE, Weinberger DR, Goldberg TE (1998) Operant conditioning and the orbitofrontal cortex in schizophrenic patients: unexpected evidence for intact functioning. Schizophr Res 30:169174.[ISI][Medline]
Wilson FAW, Scalaidhe SPO, Goldman-Rakic PS (1993) Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260:19551958.[ISI][Medline]
Zajonc RB (1984) On the primacy of affect. Am Psychol 39:117123.[ISI]