State anxiety alters the neural oscillatory correlates of predictions and prediction errors during reward-based learning

Anxiety influences how the brain estimates and responds to uncertainty. The consequences of these processes on behaviour have been described in theoretical and empirical studies, yet the associated neural correlates remain unclear. Rhythm-based accounts of Bayesian predictive coding propose that predictions in generative models of perception are represented in alpha (8–12 Hz) and beta oscillations (13–30 Hz). Updates to predictions are driven by prediction errors weighted by precision (inverse variance), and are encoded in gamma oscillations (>30 Hz) and associated with suppression of beta activity. We tested whether state anxiety alters the neural oscillatory activity associated with predictions and precision-weighted prediction errors (pwPE) during learning. Healthy human participants performed a probabilistic reward-based learning task in a volatile environment. In our previous work, we described learning behaviour in this task using a hierarchical Bayesian model, revealing more precise (biased) beliefs about the tendency of the reward contingency in state anxiety, consistent with reduced learning in this group. The model provided trajectories of predictions and pwPEs for the current study, allowing us to assess their parametric effects on the time-frequency representations of EEG data. Using convolution modelling for oscillatory responses, we found that, relative to a control group, state anxiety increased beta activity in frontal and sensorimotor regions during processing of pwPE, and in fronto-parietal regions during encoding of predictions. No effects of state anxiety on gamma modulation were found. Our findings expand prior evidence on the oscillatory representations of predictions and pwPEs into the reward-based learning domain. The results suggest that state anxiety modulates beta-band oscillatory correlates of pwPE and predictions in generative models, providing insights into the neural processes associated with biased belief updating and poorer learning

Optimized alpha band patterns correlated with trait anxiety

Anxiety is one of the most prevalent mental disorders, affecting approximately 5-10% of the adult population worldwide. It can severely impact quality of life, but also place a large burden on the health systems. Despite its omnipresence and impact on mental and physical health, most of the individuals suffering from anxiety do not receive appropriate treatment. Furthermore, while neuroimaging research consistently implicated subcortical structures such as amygdala, hippocampus and prefrontal cortex in anxiety, there is still a lack of consensus on the underlying neurophysiological processes contributing to this condition. Thus, the objective neurophysiological markers for anxiety remain elusive. Methods allowing non-invasive recording and assessment of cortical processing provide an opportunity to help identify anxiety signatures that could be used as intervention targets. In this paper, we tackle this problem by applying a regression spatial filter called Source-Power Comodulation (SPoC) to trait anxiety data of 43 individuals. By maximizing the correlation of alpha band power and the level of trait anxiety in resting state electroencephalography (EEG) we are able to obtain neurophysiologically meaningful patterns that should be helpful in the search of biomarkers for mental disorders

Identification of spatial patterns with maximum association between power of resting state neural oscillations and trait anxiety

Anxiety affects approximately 5-10% of the adult population worldwide, placing a large burden on the health systems. Despite its omnipresence and impact on mental and physical health, most of the individuals affected by anxiety do not receive appropriate treatment. Current research in the field of psychiatry emphasizes the need to identify and validate biological markers relevant to this condition. Neurophysiological preclinical studies are a prominent approach to determine brain rhythms that can be reliable markers of key features of anxiety. However, while neuroimaging research consistently implicated prefrontal cortex and subcortical structures, such as amygdala and hippocampus, in anxiety, there is still a lack of consensus on the underlying neurophysiological processes contributing to this condition. Methods allowing non-invasive recording and assessment of cortical processing may provide an opportunity to help identify anxiety signatures that could be used as intervention targets. In this study, we apply Source-Power Comodulation (SPoC) to electroencephalography (EEG) recordings in a sample of participants with different levels of trait anxiety. SPoC was developed to find spatial filters and patterns whose power comodulates with an external variable in individual participants. The obtained patterns can be interpreted neurophysiologically. Here, we extend the use of SPoC to a multi-subject setting and test its validity using simulated data with a realistic head model. Next, we apply our SPoC framework to resting state EEG of 43 human participants for whom trait anxiety scores were available. SPoC inter-subject analysis of narrow frequency band data reveals neurophysiologically meaningful spatial patterns in the theta band (4-7 Hz) that are negatively correlated with anxiety. The outcome is specific to the theta band and not observed in the alpha (8-12 Hz) or beta (13-30 Hz) frequency range. The theta-band spatial pattern is primarily localised to the superior frontal gyrus. We discuss the relevance of our spatial pattern results for the search of biomarkers for anxiety and their application in neurofeedback studies

Introspection confidence predicts EEG decoding of self-generated thoughts and meta-awareness

The neurophysiological bases of mind wandering (MW) – an experiential state wherein attention is disengaged from the external environment in favour of internal thoughts, and state meta-awareness are poorly understood. In parallel, the relationship between introspection confidence in experiential state judgements and neural representations remains unclear. Here, we recorded EEG whilst participants completed a listening task within which they made experiential state judgments and rated their confidence. Alpha power was reliably greater during MW episodes, with unaware MW further associated with greater delta and theta power. Multivariate pattern classification analysis revealed that MW, and meta-awareness can be decoded from the distribution of power in these three frequency bands. Critically, we show that individual decoding accuracies positively correlate with introspection confidence. Our results reaffirm the role of alpha oscillations in MW, implicate lower frequencies in meta-awareness, and are consistent with the proposal that introspection confidence indexes neurophysiological discriminability of representational states

Characterizing the middle-age neurophysiology using EEG/MEG

Middle adulthood – the period of life between 40 and 60 years of age – is accompanied by important physical and emotional changes, as well as cognitive and neuronal ones. Nevertheless, middle age is often overlooked in neuroscience under the assumption that this is a time of relative stability, although cognitive decline, as well as changes in brain structure and function are well-established by the age of 60. Here we characterized the middle-aged brain in the context of healthy younger and older adults by assessing resting-state electrophysiological and neuromagnetic activity in two different samples (N = 179, 631). Alpha and beta oscillations – two key ageing signatures – were analyzed in terms of spectral power and burst events. While posterior alpha power and burst rate features changed linearly with age, similarly to behavioral measures, sensorimotor beta power and burst rate properties varied non-linearly, with inflection points during middle age. The findings suggest that ageing is characterized by distinct spatial and temporal brain dynamics, some critically arising in middle age

Evaluating the Influence of Musical and Monetary Rewards on Decision Making through Computational Modelling

A central question in behavioural neuroscience is how different rewards modulate learning. While the role of monetary rewards is well-studied in decision-making research, the influence of abstract rewards like music remains poorly understood. This study investigated the dissociable effects of these two reward types on decision making. Forty participants completed two decision-making tasks, each characterised by probabilistic associations between stimuli and rewards, with probabilities changing over time to reflect environmental volatility. In each task, choices were reinforced either by monetary outcomes (win/lose) or by the endings of musical melodies (consonant/dissonant). We applied the Hierarchical Gaussian Filter, a validated hierarchical Bayesian framework, to model learning under these two conditions. Bayesian statistics provided evidence for similar learning patterns across both reward types, suggesting individuals’ similar adaptability. However, within the musical task, individual preferences for consonance over dissonance explained some aspects of learning. Specifically, correlation analyses indicated that participants more tolerant of dissonance behaved more stochastically in their belief-to-response mappings and were less likely to choose the response associated with the current prediction for a consonant ending, driven by higher volatility estimates. By contrast, participants averse to dissonance showed increased tonic volatility, leading to larger updates in reward tendency beliefs

State anxiety biases estimates of uncertainty and impairs reward learning in volatile environments

Clinical and subclinical (trait) anxiety impairs decision making and interferes with learning. Less understood are the effects of temporary anxious states on learning and decision making in healthy populations, and whether these can serve as a model for clinical anxiety. Here we test whether anxious states in healthy individuals elicit a pattern of aberrant behavioural, neural, and physiological responses comparable with those found in anxiety disorders—particularly when processing uncertainty in unstable environments. In our study, both a state anxious and a control group learned probabilistic stimulus-outcome mappings in a volatile task environment while we recorded their electrophysiological (EEG) signals. By using a hierarchical Bayesian model of inference and learning, we assessed the effect of state anxiety on Bayesian belief updating with a focus on uncertainty estimates. State anxiety was associated with an underestimation of environmental uncertainty, and informational uncertainty about the reward tendency. Anxious individuals’ beliefs about reward contingencies were more precise (had smaller uncertainty) and thus more resistant to updating, ultimately leading to impaired reward-based learning. State anxiety was also associated with greater uncertainty about volatility. We interpret this pattern as evidence that state anxious individuals are less tolerant to informational uncertainty about the contingencies governing their environment and more willing to be uncertain about the level of stability of the world itself. Further, we tracked the neural representation of belief update signals in the trial-by-trial EEG amplitudes. In control participants, lower-level precision-weighted prediction errors (pwPEs) about reward tendencies were represented in the ERP signals across central and parietal electrodes peaking at 496 ms, overlapping with the late P300 in classical ERP analysis. The state anxiety group did not exhibit a significant representation of low-level pwPEs, and there were no significant differences between the groups. Smaller variance in low-level pwPE about reward tendencies in state anxiety could partially account for the null results. Expanding previous computational work on trait anxiety, our findings establish that temporary anxious states in healthy individuals impair reward-based learning in volatile environments, primarily through changes in uncertainty estimates, which play a central role in current Bayesian accounts of perceptual inference and learning

Resting-State Theta Oscillations and Reward Sensitivity in Risk Taking

Females demonstrate greater risk aversion than males on a variety of tasks, but the underlying neurobiological basis is still unclear. We studied how theta (4–7 Hz) oscillations at rest related to three different measures of risk taking. Thirty-five participants (15 females) completed the Bomb Risk Elicitation Task (BRET), which allowed us to measure risk taking during an economic game. The Domain-Specific Risk-Taking Scale (DOSPERT) was used to measure self-assessed risk attitudes as well as reward and punishment sensitivities. In addition, the Barratt Impulsiveness Scale (BIS11) was included to quantify impulsiveness. To obtain measures of frontal theta asymmetry and frontal theta power, we used magnetoencephalography (MEG) acquired prior to task completion, while participants were at rest. Frontal theta asymmetry correlated with average risk taking during the game but only in the female sample. By contrast, frontal theta power correlated with risk taking as well as with measures of reward and punishment sensitivity in the joint sample. Importantly, we showed that reward sensitivity mediated a correlation between risk taking and the power of theta oscillations localized to the anterior cingulate cortex. In addition, we observed significant sex differences in source- and sensor-space theta power, risk taking during the game, and reward sensitivity. Our findings suggest that sensitivity to rewards, associated with resting-state theta oscillations in the anterior cingulate cortex, is a trait that potentially contributes to sex differences in risk taking

Alterations in the amplitude and burst rate of beta oscillations impair reward-dependent motor learning in anxiety

Anxiety results in sub-optimal motor learning, but the precise mechanisms through which this effect occurs remain unknown. Using a motor sequence learning paradigm with separate phases for initial exploration and reward-based learning, we show that anxiety states in humans impair learning by attenuating the update of reward estimates. Further, when such estimates are perceived as unstable over time (volatility), anxiety constrains adaptive behavioral changes. Neurally, anxiety during initial exploration increased the amplitude and the rate of long bursts of sensorimotor and prefrontal beta oscillations (13–30 Hz). These changes extended to the subsequent learning phase, where phasic increases in beta power and burst rate following reward feedback were linked to smaller updates in reward estimates, with a higher anxiety-related increase explaining the attenuated belief updating. These data suggest that state anxiety alters the dynamics of beta oscillations during reward processing, thereby impairing proper updating of motor predictions when learning in unstable environments

Unsupervised statistical learning underpins computational, behavioural, and neural manifestations of musical expectation

The ability to anticipate forthcoming events has clear evolutionary advantages, and predictive successes or failures often entail significant psychological and physiological consequences. In music perception, the confirmation and violation of expectations are critical to the communication of emotion and aesthetic effects of a composition. Neuroscientific research on musical expectations has focused on harmony. Although harmony is important in Western tonal styles, other musical traditions, emphasizing pitch and melody, have been rather neglected. In this study, we investigated melodic pitch expectations elicited by ecologically valid musical stimuli by drawing together computational, behavioural, and electrophysiological evidence. Unlike rule-based models, our computational model acquires knowledge through unsupervised statistical learning of sequential structure in music and uses this knowledge to estimate the conditional probability (and information content) of musical notes. Unlike previous behavioural paradigms that interrupt a stimulus, we devised a new paradigm for studying auditory expectation without compromising ecological validity. A strong negative correlation was found between the probability of notes predicted by our model and the subjectively perceived degree of expectedness. Our electrophysiological results showed that low-probability notes, as compared to high-probability notes, elicited a larger (i) negative ERP component at a late time period (400–450 ms), (ii) beta band (14–30 Hz) oscillation over the parietal lobe, and (iii) long-range phase synchronization between multiple brain regions. Altogether, the study demonstrated that statistical learning produces information-theoretic descriptions of musical notes that are proportional to their perceived expectedness and are associated with characteristic patterns of neural activity