No abstract

Deciding advantageously in a complex situation is thought to require overt reasoning on declarative knowledge, namely, on facts pertaining to premises, options for action, and outcomes of actions that embody the pertinent previous experience. An alternative possibility was investigated: that overt reasoning is preceded by a nonconscious biasing step that uses neural systems other than those that support declarative knowledge. Normal participants and patients with prefrontal damage and decision-making defects performed a gambling task in which behavioral, psychophysiological, and self-account measures were obtained in parallel. Normals began to choose advantageously before they realized which strategy worked best, whereas prefrontal patients continued to choose disadvantageously even after they knew the correct strategy. Moreover, normals began to generate anticipatory skin conductance responses (SCRs) whenever they pondered a choice that turned out to be risky, before they knew explicitly that it was a risky choice, whereas patients never developed anticipatory SCRs, although some eventually realized which choices were risky. The results suggest that, in normal individuals, nonconscious biases guide behavior before conscious knowledge does. Without the help of such biases, overt knowledge may be insufficient to ensure advantageous behavior.

The somatic marker hypothesis provides a systems-level neuroanatomical and cognitive framework for decision making and the influence on it by emotion. The key idea of this hypothesis is that decision making is a process that is influenced by marker signals that arise in bioregulatory processes, including those that express themselves in emotions and feelings. This influence can occur at multiple levels of operation, some of which occur consciously and some of which occur non-consciously. Here we review studies that confirm various predictions from the hypothesis. The orbitofrontal cortex represents one critical structure in a neural system subserving decision making. Decision making is not mediated by the orbitofrontal cortex alone, but arises from large-scale systems that include other cortical and subcortical components. Such structures include the amygdala, the somatosensory/insular cortices and the peripheral nervous system. Here we focus only on the role of the orbitofrontal cortex in decision making and emotional processing, and the relationship between emotion, decision making and other cognitive functions of the frontal lobe, namely working memory.

The somatic marker hypothesis proposes that decision-making is a process that depends on emotion. Studies have shown that damage of the ventromedial prefrontal (VMF) cortex precludes the ability to use somatic (emotional) signals that are necessary for guiding decisions in the advantageous direction. However, given the role of the amygdala in emotional processing, we asked whether amygdala damage also would interfere with decision-making. Furthermore, we asked whether there might be a difference between the roles that the amygdala and VMF cortex play in decision-making. To address these two questions, we studied a group of patients with bilateral amygdala, but not VMF, damage and a group of patients with bilateral VMF, but not amygdala, damage. We used the "gambling task" to measure decision-making performance and electrodermal activity (skin conductance responses, SCR) as an index of somatic state activation. All patients, those with amygdala damage as well as those with VMF damage, were (1) impaired on the gambling task and (2) unable to develop anticipatory SCRs while they pondered risky choices. However, VMF patients were able to generate SCRs when they received a reward or a punishment (play money), whereas amygdala patients failed to do so. In a Pavlovian conditioning experiment the VMF patients acquired a conditioned SCR to visual stimuli paired with an aversive loud sound, whereas amygdala patients failed to do so. The results suggest that amygdala damage is associated with impairment in decision-making and that the roles played by the amygdala and VMF in decision-making are different.

On a gambling task that models real-life decisions, patients with bilateral lesions of the ventromedial prefrontal cortex (VM) opt for choices that yield high immediate gains in spite of higher future losses. In this study, we addressed three possibilities that may account for this behaviour: (i) hypersensitivity to reward; (ii) insensitivity to punishment; and (iii) insensitivity to future consequences, such that behaviour is always guided by immediate prospects. For this purpose, we designed a variant of the original gambling task in which the advantageous decks yielded high immediate punishment but even higher future reward. The disadvantageous decks yielded low immediate punishment but even lower future reward. We measured the skin conductance responses (SCRs) of subjects after they had received a reward or punishment. Patients with VM lesions opted for the disadvantageous decks in both the original and variant versions of the gambling task. The SCRs of VM lesion patients after they had received a reward or punishment were not significantly different from those of controls. In a second experiment, we investigated whether increasing the delayed punishment in the disadvantageous decks of the original task or decreasing the delayed reward in the disadvantageous decks of the variant task would shift the behaviour of VM lesion patients towards an advantageous strategy. Both manipulations failed to shift the behaviour of VM lesion patients away from the disadvantageous decks. These results suggest that patients with VM lesions are insensitive to future consequences, positive or negative, and are primarily guided by immediate prospects. This 'myopia for the future' in VM lesion patients persists in the face of severe adverse consequences, i.e. rising future punishment or declining future reward.

In a series of [15O]PET experiments aimed at investigating the neural basis of emotion and feeling, 41 normal subjects recalled and re-experienced personal life episodes marked by sadness, happiness, anger or fear. We tested the hypothesis that the process of feeling emotions requires the participation of brain regions, such as the somatosensory cortices and the upper brainstem nuclei, that are involved in the mapping and/or regulation of internal organism states. Such areas were indeed engaged, underscoring the close relationship between emotion and homeostasis. The findings also lend support to the idea that the subjective process of feeling emotions is partly grounded in dynamic neural maps, which represent several aspects of the organism's continuously changing internal state.

Studies in animals have shown that the amygdala receives highly processed visual input, contains neurons that respond selectively to faces, and that it participates in emotion and social behaviour. Although studies in epileptic patients support its role in emotion, determination of the amygdala's function in humans has been hampered by the rarity of patients with selective amygdala lesions. Here, with the help of one such rare patient, we report findings that suggest the human amygdala may be indispensable to: (1) recognize fear in facial expressions; (2) recognize multiple emotions in a single facial expression; but (3) is not required to recognize personal identity from faces. These results suggest that damage restricted to the amygdala causes very specific recognition impairments, and thus constrains the broad notion that the amygdala is involved in emotion.

Two parallel studies using positron emission tomography, one conducted in neurological patients with brain lesions, the other in normal individuals, indicate that the normal process of retrieving words that denote concrete entities depends in part on multiple regions of the left cerebral hemisphere, located outside the classic language areas. Moreover, anatomically separable regions tends to process words for distinct kinds of items.