Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making

Abstract

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.

Fig. 1.

Neuroanatomical findings in the two groups of brain-damaged patients. A, Bilateral amygdala lesions. Coronal sections through the amygdala from the three patients in our Registry show complete bilateral destruction of the amygdala. The lesions from the two remaining amygdala patients have been shown in previous publications (Lee et al., 1988a,b, 1995). B, Bilateral VMF lesions. Shown are mesial and inferior views of the overlap of lesions from four VMF patients. The lesions from individual subjects were transferred onto a reference brain by using the MAP-3 technique (Frank et al., 1997). The coronal section shows an area of the ventromedial prefrontal cortex where maximum overlap occurs. The position of the cut is indicated on the brain on theleft. The color bar below shows the color code corresponding to the number of overlapping lesions. The lesion of the fifth VMF patient is not part of the MAP-3 image because, as explained in the text, this patient suffered from a frontal lobe cyst at age 2. The lack of a clear structural lesion at macroscopic level precludes the transfer into MAP-3.

Fig. 2.

Means ± SEM of the total number of cards selected from the advantageous versus the disadvantageous decks in each block of 20 cards, which were made by normal controls and by patients with bilateral amygdala or VMF cortex lesions. It is shown that control subjects learn to avoid the bad decks and prefer the good decks. Amygdala and VMF patients fail to do so.

Fig. 3.

Means ± SEM of anticipatory SCRs (μS/sec) generated by controls, amygdala, or VMF patients in association with the advantageous decks (C and D, white columns) versus the disadvantageous decks (A and B, black columns).

Fig. 4.

Means ± SEM of reward and punishment SCRs (μS/sec) generated by controls, amygdala, or VMF patients in association with the advantageous decks (C and D, white columns) or the disadvantageous decks (A and B, black columns).

Fig. 5.

A, Magnitudes of SCRs in the conditioning phase as compared with the SCRs in the habituation and extinction phases. Each point on the plot represents the means ± SEM of the magnitudes of SCRs generated by control subjects, amygdala, and VMF patients during each phase of the conditioning experiment. Each Habituation score represents the mean (from n = 6 controls, 5 VMF, and 5 amygdala patients) of the mean magnitude of SCRs generated in response to the last three slides preceding conditioning. EachConditioning score represents the mean of the mean magnitude of SCRs generated in response to six presentations of the CS (not followed by the US). Each Extinction 1 score represents the mean of the mean magnitude of SCRs generated in response to the first three repeated presentations of the CS during extinction. Each Extinction 2 score represents the mean of the mean magnitude of SCRs in response to the last three repeated presentations of the CS. B, Magnitudes of SCRs to the blue slides (CS) that were paired with the US during conditioning. Eachcolumn represents the mean ± SEM of the mean magnitude of SCRs generated in response to six presentations of the CS (paired with the US) from the same control subjects and brain-damaged patients as in A.