Losses resulting from deliberate exploration trigger beta oscillations in frontal cortex

Abstract

We examined the neural signature of directed exploration by contrasting MEG beta (16–30 Hz) power changes between disadvantageous and advantageous choices in the two-choice probabilistic reward task. We analyzed the choices made after the participants have learned the probabilistic contingency between choices and their outcomes, i.e., acquired the inner model of choice values. Therefore, rare disadvantageous choices might serve explorative, environment-probing purposes. The study brought two main findings. Firstly, decision making leading to disadvantageous choices took more time and evidenced greater large-scale suppression of beta oscillations than its advantageous alternative. Additional neural resources recruited during disadvantageous decisions strongly suggest their deliberately explorative nature. Secondly, an outcome of disadvantageous and advantageous choices had qualitatively different impact on feedback-related beta oscillations. After the disadvantageous choices, only losses—but not gains—were followed by late beta synchronization in frontal cortex. Our results are consistent with the role of frontal beta oscillations in the stabilization of neural representations for selected behavioral rule when explorative strategy conflicts with value-based behavior. Punishment for explorative choice being congruent with its low value in the reward history is more likely to strengthen, through punishment-related beta oscillations, the representation of exploitative choices consistent with the inner utility model.

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

“…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.…”

“…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.…”

Atypical Pupil-Linked Arousal Induced by Low-Risk Probabilistic Choices, and Intolerance of Uncertainty in Adults with ASD

“…Nevertheless, participants still make rare disadvantageous choices, probably in a purposeful search for information, at the cost of not using the option that is currently judged to be better. In favor of this assumption was the fact that risky exploratory versus safe exploitative decisions were associated with simultaneous increases in post-decision pupil dilation, increased decision-related brain activation, and slower decision times (Chernyshev et al, 2023; Kozunova et al, 2022). Thus, neurotypical subjects can optimally scale their subjective uncertainty, i.e., reduce decision time, brain activity, and autonomic arousal when choosing an option that has been frequently rewarded in the past (i.e., exploitative choice), while maintaining high phasic arousal and prolonged decision time when making a deliberate risky choice that conflicts with the model-based prediction (i.e., a directed exploratory choice).…”