Neurophysiological mechanisms of exploration and exploitation in high-functioning autism: Magnetoencephalographic study

Abstract

Intolerance of uncertainty and high sensitivity to the threat of failure are believed to contribute to chronic anxiety in individuals with high-functioning autism. This study examines the influence of these personality traits on the brain processes involved in decision-making in a probabilistic setting among autism patients. Furthermore, we explore the causal relationship between these personality traits and chronic anxiety in individuals with high-functioning autism. Twenty-one high-functioning autistic individuals who are intolerant to uncertainty, aged 19 to 46, and 21 neurotypical volunteers of the same age, carried out a probabilistic choice experiment with two alternatives. One option yielded a monetary profit of 70% of the time, while the other brought only a 30% gain. Following each selection, the subjects received feedback on their decision and gradually learned, through trial and error, to prefer the more advantageous option. From this point forward, we consider frequent selections of a beneficial stimulus to align with the internal utility model, specifically the exploitation strategy. On the other hand, sporadic choices of a detrimental stimulus correspond to an exploration strategy, which may prove disadvantageous in a stable environment but enables adaptation to unforeseen changes in the surroundings. We hypothesized that there are characteristic differences in brain activity reflecting exploration and exploitation strategies between groups, which would emerge during the decision-making period and after internal feedback evaluation regarding advantageous and disadvantageous choices [1]. Beta oscillations (16–30 Hz) were analyzed in the magnetoencephalographic recordings. The decrease in beta oscillation power below baseline during the period between stimulus presentation and subjects’ response indicates activation in brain regions related to decision-making strategy. Conversely, an increase in beta oscillation power following feedback signaling a disadvantageous choice reflects a mechanism that reinforces internal value models in current task conditions [1]. The cortical sources of beta oscillations in 448 cortical areas were estimated using the sLoreta technique at the single-trial level. Mixed linear models (LMM) were used for statistical analysis with correction for multiple comparisons via the FDR method for the number of cortical areas analyzed. The study concentrated on the time interval for decision-making (–900 to –300 ms prior to the motor action of choice) and the post-feedback period (500 to 900 ms after the commencement of the feedback presentation) [1]. Based on questionnaire results, individuals with high-functioning autism exhibited a significantly lower tolerance for uncertainty and a greater intolerance for uncertainty when compared to neurotypical participants. The study generated two primary findings. Initially, the extent of brain activity during decision-making differed in control subjects and subjects with autism based on the type of choice, with exact opposition. Opting for an advantageous vs. disadvantageous choice was linked with reduced activation of the inferior temporal, parietal, and medial frontal cortex regions in control subjects and elevated activation in these regions for subjects with autism spectrum disorder. These findings suggest that neurotypical individuals utilize fewer neural resources and exhibit decreased emotional response while deciding in favor of a known profitable outcome compared to opting for an uncertain choice — one that is more likely to result in a negative outcome based on previous experiences. Individuals with autism allocate disproportionate amounts of attention and emotional resources towards planning actions that are deemed safe and offer only a probable (though not definite) advantage. Conversely, the prospect of failure due to risky behavior induces a comparatively muted response in their brains. Second, our internal evaluation of feedback focused on variations in functional activity within the orbitofrontal and lateral prefrontal cortical areas during exploratory (disadvantageous) choices between individuals with autism and control subjects. As previously reported, neurotypical subjects demonstrated significant beta synchronization following negative feedback after disadvantageous choices [1]. Contrary to control participants, individuals with autism spectrum disorder exhibited a lack of synchronization in frontal beta oscillations following losses incurred from unfavorable selections. This observation may indicate insufficient reinforcement of the internal utility model, which typically strengthens in response to negative outcomes that align with predicted results [1]. Overall, our study found that individuals on the autism spectrum with a high intolerance for uncertainty exhibit significantly increased activation of brain decision-making systems in situations that are perceived to be low-risk and with a high probability of a successful outcome. These findings clarify the reasons behind the puzzling rise in anxiety and autonomic reactivity among individuals in situations where they anticipate rewards, which are not inherently aversive unlike fear of punishment [2].