The role of emotion in decision-making: Evidence from neurological patients with orbitofrontal damage
Introduction
The orbitofrontal region of the prefrontal cortex includes the rectus gyrus and orbital gyri, which constitute the inferior surface of the frontal lobes lying immediately above the orbital plates. Lesions of this region are not usually restricted to the orbitofrontal cortex, but they extend into neighboring cortex and involve different size sectors of the ventromedial prefrontal (VM) region. The VM region includes the medial and varying sectors of the lateral orbitofrontal cortex, thus encompassing Brodmann’s areas (BA) 25, lower 24, 32, and medial aspect of 11, 12, and 10, and the white matter subjacent to all of these areas. Patients with bilateral lesions of the VM cortex (Fig. 1) develop severe impairments in personal and social decision-making, in spite of otherwise largely preserved intellectual abilities. Before their brain damage, they have normal intelligence and creativity. After the damage, they develop difficulties in planning their workday and future; difficulties in choosing friends, partners, and activities (Bechara, Damasio et al., 2000; Bechara, Tranel, & Damasio, 2002).
The “Somatic Marker Hypothesis” was proposed in order to provide a neural explanation of the real-life decision-making defect of these patients. The main point of this hypothesis is that decision-making is a process guided by emotions. There is a link between the abnormalities in emotion and feeling of these patients and their severe impairment in judgment and decision-making in real-life (Bechara, Damasio et al., 2000, Bechara et al., 2002).
We tested the somatic marker hypothesis using the gambling task (GT) paradigm for measuring decision-making (Bechara, Tranel, & Damasio, 2000). However, there are other paradigms, namely the “betting task” (also referred to as the Cambridge Gamble Task) developed by Rogers and colleagues (Rogers, Everitt et al., 1999), and tasks of delayed discounting (Bickel, Degrandpre, & Higgins, 1995). It has been shown that there is a significant correlation between performance on the GT, the “betting task,” and tasks of delayed discounting (Monterosso, Ehrman, Napier, O’Brien, & Childress, 2001), thus supporting the notion that these three sets of tasks may engage a common mechanism of decision-making, tied to the VM region.
Section snippets
The gambling task
The task has been described in detail elsewhere (Bechara, Tranel et al., 2000). Briefly, in the gambling task (also referred to as the Iowa gambling task), subjects have to choose between decks of cards which yield high immediate gain but larger future loss, i.e., long term loss, and decks which yield lower immediate gain but a smaller future loss, i.e., a long term gain. The task consists of four decks of cards named A, B, C, and D. The goal in the task is to maximize profit on a loan of play
Behavioral findings in VM patients
We investigated the performance of normal control subjects with demographic characteristics matched to a group of patients with bilateral damage to the VM region of the prefrontal cortex (Fig. 1) and a separate group of patients with damage to the lateral occipital or lateral temporal cortex (brain-damaged controls). Normal and brain-damaged control subjects avoided the bad/disadvantageous decks (A and B) and preferred the good decks (C and D). By contrast, VM patients did not avoid (i.e., they
Right versus left VM damage
Given the functional asymmetry of the cerebral hemispheres, it is important to determine whether the decision-making deficit associated with damage to the VM prefrontal cortex is caused mostly by unilateral right or left lesions. Unfortunately, this question has been difficult to address with lesion studies, because of the rarity of patients who have a unilateral damage on the medial and orbital side of the prefrontal cortex. We have collected data from such rare patients with right or left VM
Developmental versus adult onset of VM damage
Patients who acquired VM prefrontal lobe damage during childhood are relatively rare. However, evidence from two young adults who acquired focal damage to the prefrontal cortex in early childhood, prior to 16 months of age, revealed very important facts (Anderson, Bechara, Damasio, Tranel, & Damasio, 1999). The patients with early-onset VM lesions superficially resemble adult-onset patients in terms of disrupted social behavior, which contrasts with normal basic cognitive abilities. These
Peripheral mechanisms of decision-making
The key idea of the somatic marker 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. What is the evidence that supports the notion that physiological changes related to emotion (somatic states), which arise in the body outside the brain, do play a role in influencing decisions?
There are three possible neural routes by which somatic signals expressed in the
Decision-making versus other frontal lobe functions
In a series of studies with non-human primates and human subjects, Petrides, 1985, Petrides, 1990 has established a link between frontal lobe damage and learning conditional associations, i.e., the ability to associate responses with specific stimuli on the basis of repeated feedback. However, closer investigations revealed that the posterior DL sector may be the critical region for this function. Shallice and colleagues have attempted to investigate deficits in planning ability associated with
Decision-making and working memory are mediated by separate anatomical sectors
The frontal lobe function that we addressed in detail in relation to decision-making is working memory. The rationale for the notion that working memory and decision-making are distinct functions comes from the observations that VM patients suffer from impairments in decision-making, while preserving a normal level of memory and intellect. On the other hand, although some patients with lesions in the dorsolateral sector of the prefrontal cortex (DLPC) complain of memory impairments, they do not
Decision-making versus impulse control or response inhibition
Working memory includes several components, e.g., short-term storage, rehearsal, and executive processes operating on the contents of storage (Smith, 2000; Smith & Jonides, 1999). The DLPC appears involved specifically in the executive process of working memory, i.e., the monitoring of mnemonic operations rather than the short-term storage of information (Petrides, 2000; Petrides, Alivisatos, & Frey, 2002). Neurons in DLPC project to the hippocampal region and the overlaying temporal cortices,
Conclusions
The somatic marker hypothesis provides a systems-level neuroanatomical and cognitive framework for decision-making and its influence 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. The orbitofrontal cortex represents one critical structure in a neural system subserving decision-making. However, the orbitofrontal cortex
Developmental implications
The functions of the prefrontal cortex may not develop fully until the age of 21 (Begley, 2000; Rubia et al., 2000). During this period, the development of neural connections that underlie more complex behaviors, including decision-making and the control over powerful temptations, is still taking place (Eslinger, 1999). There are several pre-existing factors that may promote abnormal development of the prefrontal cortex and its connectivity during this vulnerable period of development. Some of
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