The Contribution of Distinct Subregions of the Ventromedial Frontal Cortex to Emotion, Social Behavior, and Decision Making
Rudebeck, P. H., Bannerman, D. M., Rushworth, M. F. S., Cognitive, Affective and Behavioral Neuroscience
Damage to the ventromedial frontal cortex (VMFC) in humans is associated with deficits in decision making. Decision making, however, often happens while people are interacting with others, where it is important to take the social consequences of a course of action into account. It is well known that VMFC lesions also lead to marked alterations in patients' emotions and ability to interact socially; however, it has not been clear which parts of the VMFC are critical for these changes. Recently, there has been considerable interest in the role of the VMFC in choice behavior during interpersonal exchanges. Here, we highlight recent research that suggests that two areas within or adjacent to the VMFC, the orbitofrontal cortex (OFC) and the anterior cingulate cortex (ACC), may play distinct but complementary roles in mediating normal patterns of emotion and social behavior. Converging lines of evidence from human, macaque, and rat studies now suggest that the OFC may be more specialized for simple emotional responses, such as fear and aggression, through its role in representing primary reinforcement or punishment. By contrast, the ACC may play a distinct role in more complex aspects of emotion, such as social interaction, by virtue of its connections with the discrete parts of the temporal lobe and subcortical structures that control autonomic responses.
Psychologists and neuroscientists the world over know the remarkable story of Phineas Gage. While using a tamping iron to push an explosive charge into solid rock, Gage set off an uncontrolled explosion that drove the iron into the left side of his cranium, damaging his ventromedial frontal cortex (VMFC; H. Damasio, Grabowski, Frank, Galaburda, & Damasio, 1994; Harlow, 1848). Although accidents on the railroad construction sites of 19th century America were probably common, this case is famous not only because Gage survived, but also because the changes in his personality following the accident were so well documented (Harlow, 1848, 1868). Over the next 12 years until Gage's death, John Harlow recorded the severe changes in decision making and personality that followed the accident (cf. Macmillan, 2002). These records provided the first evidence that a part of the frontal lobe is crucial for preferentially guiding our choices, but also for regulating our emotions and social interactions.
More recently, researchers have been able to further characterize the role of the VMFC in social interaction, emotion, and decision making through work with human patients and animals with damage similar to that suffered by Gage (Bechara, Damasio, & Damasio, 2000; Murray & Izquierdo, 2007). From these studies, there has been considerable interest in the contribution of the VMFC to decision making, especially the role of this area in mediating the influence of emotion on decision making (Bechara, Damasio, Damasio, & Anderson, 1994; Bechara et al., 2000; Bechara, Damasio, Tranel, & Damasio, 1997). In their now seminal series of studies, Bechara and colleagues showed that patients with VMFC damage fail to advantageously alter their pattern of choices in a probabilistic game for monetary reward called the Iowa gambling task (IGT; Bechara et al., 1994). Specifically, in comparison with control subjects, patients with VMFC lesions continue to make risky instead of safe choices, even after they have incurred substantial losses. On the basis of additional experiments. it was proposed that patients' disadvantageous pattern of choices may be related to an inability to unconsciously use visceral sensations (somatic markers) to preferentially guide choices (Bechara et al., 1997).
Although it is still acknowledged that VMFC patients perform poorly on a range of decision-making tests (Camille et al., 2004; Wheeler & Fellows, 2008), there is now considerable debate concerning the precise role of somatic markers in the patients' decision-making impairments. During the IGT, people with VMFC damage are able to report which are the safe, as opposed to the risky, choices. …