Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making

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.

Oxytocin facilitates protective responses to aversive social stimuli in males

“…In addition to empathy and compassion, the anterior insula has been implicated in interoceptive awareness and estimation of uncertainty and risk (44,(51)(52)(53)(54)(55). In the context of our experiments the effects of OXT in increasing the impact of aversive social information may reflect enhanced perception of visceral reactions and feelings of uncertainty and risk arising from elevated empathic responses, promoting approach and protective behavior toward individuals exposed to social threat.…”

Punishment and psychopathy: a case-control functional MRI investigation of reinforcement learning in violent antisocial personality disordered men

“…34 Insular damage in human beings promotes risky decision-making because of impaired signalling of the probability of aversive outcomes. 35 Reductions in grey-matter volume in the insula have been reported in adults with psychopathy, 7,29 as have reductions in insula activity during aversive conditioning 30 and atypically increased activation in response to empathy-eliciting scenarios. 8 Regions involved in representing subjective value, such as the ventromedial prefrontal cortex and posterior cingulate cortex, have been proposed to integrate input from the superior temporal gyrus.…”

Damage to insula abolishes cognitive distortions during simulated gambling

“…This approach maximizes power to detect an effect in regions that are anatomically interconnected, and likely to operate as a functional circuit (26). At a second stage of analysis, the target group was separated into the constituent subgroups to directly compare the effects of vmPFC, insula, and amygdala damage, given evidence for differential functional specializations of these regions (29)(30)(31). In both analyses, the groups did not differ significantly in terms of age, years of education, or sex distribution (Table S1).…”

“…Such predictions about the uncertainty of the environment are relevant to the near-miss effect (51) and gambler's fallacy (35), and arguably less relevant to the illusion of control effect that did not vary across lesion groups here. Past work in cases with insula lesions has shown increases in risktaking and impaired discrimination between risky gains and risky losses (31,52). By using an investment task in which most participants are loss-averse, patients with brain injury to vmPFC, insula, or amygdala achieved higher profits (26), and these effects were strongest in the insula subgroup (n = 4), who also failed to modify their investment behavior as a function of prior outcome (i.e., losses vs. wins)-an effect that resembles the abolition of the gambler's fallacy (Table S5 also displays an analogous effect in icon selection on the slot machine task).…”