Intracerebral mechanisms explaining the impact of incidental feedback on mood state and risky choice

Abstract

Identifying factors whose fluctuations are associated with choice inconsistency is a major issue for rational decision theory. Here, we investigated the neuro-computational mechanisms through which mood fluctuations may bias human choice behavior. Intracerebral EEG data were collected in a large group of subjects (n = 30), while they were performing interleaved quiz and choice tasks that were designed to examine how a series of unrelated feedbacks affects decisions between safe and risky options. Neural baseline activity preceding choice onset was confronted first to mood level, estimated by a computational model integrating the feedbacks received in the quiz task, and then to the weighting of option attributes, in a computational model predicting risk attitude in the choice task. Results showed that 1) elevated broadband gamma activity (BGA) in the ventromedial prefrontal cortex (vmPFC) and dorsal anterior insula (daIns) was respectively signaling periods of high and low mood, 2) increased vmPFC and daIns BGA respectively promoted and tempered risk taking by overweighting gain versus loss prospects. Thus, incidental feedbacks induce brain states that correspond to different moods and bias the evaluation of risky options. More generally, these findings might explain why people experiencing positive (or negative) outcome in some part of their life tend to expect success (or failure) in any other.

Direct stimulation of anterior insula and ventromedial prefrontal cortex disrupts economic choices

“…An emerging consensus is that the vmPFC and aIns may play opposing roles during economic decisions, mood, or learning, with neural activity in the vmPFC associated with increased risk-seeking, pleasantness, reward-based learning and good mood (Engelmann & Tamir, 2009; Gueguen et al, 2021; Tobler et al, 2007; Venkatraman et al, 2009; Xue et al, 2009), whereas neural activity in the aIns has been linked to risk-averse decisions, unpleasantness, punishment-avoidance, and bad mood (Cecchi et al, 2022; Kuhnen & Knutson, 2005; Paulus et al, 2003; Pessiglione et al, 2006; Rolls et al, 2008; Rudorf et al, 2012; Venkatraman et al, 2009; Vinckier et al, 2018). Our findings demonstrate the causal role of aIns and vmPFC functional subregions during choices and confidence.…”

“…Choices were fitted using a published computational framework (Cecchi et al, 2022; Vinckier et al, 2018) on additional behavioral data acquired separately from 10 of 15 subjects (128 or 192 trials of the task without stimulation). Acceptance probability was calculated as a sigmoid function (softmax) of expected utility: where k t is a free parameter that accounts for a linear drift with time (trial index t ) to capture fatigue effects.…”

“…Functional imaging and intracranial electrophysiological evidence suggest that the ventromedial prefrontal cortex (vmPFC) and the anterior insular cortex (aIns) play critical roles in shaping these decisions. Accordingly, increased pre-stimulus neural activity in the vmPFC and aIns has been shown to promote and temper risk-taking, respectively, by overweighting the prospects of monetary gain or loss (Cecchi et al, 2022; Vinckier et al, 2018). Although the timing of these activities suggests a possible causal relationship between these brain regions and choice behavior, the correlational nature of the techniques used to date prevents conclusive establishment of this causal relationship.…”

“…To address these challenges, we conducted an experiment using intracranial electrical stimulation (iES) over human cortex to determine whether iES can disrupt choice behavior and also confidence judgments using a previously validated accept/reject task (Cecchi et al, 2022; Vinckier et al, 2018). Previous research has indicated that iES of the ventral aIns elicits disgust behavior or depressed affect (Caruana et al, 2011; Jezzini et al, 2012; Krolak-Salmon et al, 2003; Singh et al, 2021), whereas iES of the dorsal aIns elicits overwhelming ecstatic sensations or ingestive behavior, such as chewing and swallowing (Bartolomei et al, 2019; Jezzini et al, 2012; Nencha et al, 2022; Picard et al, 2013).…”

“…Next, we investigate the computational mechanisms through which iES disrupted choice behavior by fitting the choice data with a model based on expected utility theory (Cecchi et al, 2022; Vinckier et al, 2018). Our findings revealed that iES modulated participants’ sensitivity to potential losses (captured by the parameter kl ) in both brain regions ( Figure 2d ), but not their sensitivity to potential gains ( Supplementary Figure 2 ).…”