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, 131 (Pt 5), 1311-22

Differential Effects of Insular and Ventromedial Prefrontal Cortex Lesions on Risky Decision-Making

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Differential Effects of Insular and Ventromedial Prefrontal Cortex Lesions on Risky Decision-Making

L Clark et al. Brain.

Abstract

The ventromedial prefrontal cortex (vmPFC) and insular cortex are implicated in distributed neural circuitry that supports emotional decision-making. Previous studies of patients with vmPFC lesions have focused primarily on decision-making under uncertainty, when outcome probabilities are ambiguous (e.g. the Iowa Gambling Task). It remains unclear whether vmPFC is also necessary for decision-making under risk, when outcome probabilities are explicit. It is not known whether the effect of insular damage is analogous to the effect of vmPFC damage, or whether these regions contribute differentially to choice behaviour. Four groups of participants were compared on the Cambridge Gamble Task, a well-characterized measure of risky decision-making where outcome probabilities are presented explicitly, thus minimizing additional learning and working memory demands. Patients with focal, stable lesions to the vmPFC (n = 20) and the insular cortex (n = 13) were compared against healthy subjects (n = 41) and a group of lesion controls (n = 12) with damage predominantly affecting the dorsal and lateral frontal cortex. The vmPFC and insular cortex patients showed selective and distinctive disruptions of betting behaviour. VmPFC damage was associated with increased betting regardless of the odds of winning, consistent with a role of vmPFC in biasing healthy individuals towards conservative options under risk. In contrast, patients with insular cortex lesions failed to adjust their bets by the odds of winning, consistent with a role of the insular cortex in signalling the probability of aversive outcomes. The insular group attained a lower point score on the task and experienced more 'bankruptcies'. There were no group differences in probability judgement. These data confirm the necessary role of the vmPFC and insular regions in decision-making under risk. Poor decision-making in clinical populations can arise via multiple routes, with functionally dissociable effects of vmPFC and insular cortex damage.

Figures

Fig. 1
Fig. 1
Lesion overlap in the vmPFC lesion group, in views of the right and left lateral surfaces, and coronal sections at three points moving from anterior (1) to posterior (3) within the frontal lobes. The colour bar indicates the number of overlapping cases at each voxel. There is maximal lesion overlap across the group in the ventral and medial aspect of the prefrontal cortex, comprising Brodmann areas 10, 11, 13, 14, 25 and 32. There was no damage to the insular cortex (IN).
Fig. 2
Fig. 2
Lesion overlap in the insular cortex lesion group, in views of the right and left lateral surfaces, and coronal slices at three points moving anterior (1) to posterior (3) within the insular–somatosensory region. The colour bar indicates the number of overlapping cases at each voxel. Whilst all cases had unilateral lesions, the area of damage in the right- and left-sided cases was highly symmetrical. There is maximal lesion overlap across the group in the anterior insular cortex and somatosensory SII region, extending posteriorly into the inferior parietal cortex in some subjects.
Fig. 3
Fig. 3
Schematic showing the screen display for the Cambridge Gamble Task.
Fig. 4
Fig. 4
The effect of ratio on betting behaviour in the four groups of participants: healthy controls, vmPFC lesions, insular cortex lesions and the lesion control group.
Fig. 5
Fig. 5
(A) Increased betting behaviour (collapsed across the ascending and descending conditions, and the ratio of boxes) in both the vmPFC and insular cortex lesion groups. Statistical differences against pooled control group: *P < 0.05 **P < 0.005. (B) Risk adjustment (calculated by the equation 2a + bc2d, where a is the mean bet at the 9 : 1 ratio, b is the mean bet as the 8 : 2 ratio, etc.) collapsed across ascending and descending conditions, was selectively reduced in the insular cortex lesion group: these patients moderated their betting less as a function of the ratio of boxes than the other groups. **P < 0.005 against pooled control group. (C) The insular cortex lesion group experienced significantly more bankruptcies than healthy controls, where the total points dropped to 1 point within a block (Mann–Whitney non-parametric test **P < 0.005). (D) All groups placed higher bets in the descending condition (where the initial bets offered are high) than the ascending condition (where the initial bets offered are low), but the extent of this delay aversion did not differ between groups.
Fig. 6
Fig. 6
(A) Proportion of choices of the box colour ‘blue’ as a function of the number of red boxes in the array (1–9), in the vmPFC, insular cortex, lesion control and healthy control groups. When blue boxes were in the majority (i.e. number of red boxes was 1–4), subjects in all four groups reliably selected ‘blue’. When red boxes were in the majority (i.e. number of red boxes was 6–9), subjects in all four groups reliably selected ‘red’. Given this intact processing of basic trial-by-trial probabilities, the differences in betting behaviour in the vmPFC and insular cortex groups are assumed to reflect differences in risk processing. (B) Decision latencies (in milliseconds) to select ‘red’ or ‘blue’ as a function of the number of red boxes in the array (1–9).

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