Modulating hierarchical learning by high-definition transcranial alternating current stimulation at theta frequency.

Considerable evidence highlights the dorsolateral prefrontal cortex (DLPFC) as a key region for hierarchical (i.e. multilevel) learning. In a previous electroencephalography (EEG) study, we found that the low-level prediction errors were encoded by frontal theta oscillations (4-7 Hz), centered on right DLPFC (rDLPFC). However, the causal relationship between frontal theta oscillations and hierarchical learning remains poorly understood. To investigate this question, in the current study, participants received theta (6 Hz) and sham high-definition transcranial alternating current stimulation (HD-tACS) over the rDLPFC while performing the probabilistic reversal learning task. Behaviorally, theta tACS induced a significant reduction in accuracy for the stable environment, but not for the volatile environment, relative to the sham condition. Computationally, we implemented a combination of a hierarchical Bayesian learning and a decision model. Theta tACS induced a significant increase in low-level (i.e. probability-level) learning rate and uncertainty of low-level estimation relative to sham condition. Instead, the temperature parameter of the decision model, which represents (inverse) decision noise, was not significantly altered due to theta stimulation. These results indicate that theta frequency may modulate the (low-level) learning rate. Furthermore, environmental features (e.g. its stability) may determine whether learning is optimized as a result.

Alpha oscillations encode Bayesian belief updating underlying attentional allocation in dynamic environments.

In a dynamic environment, expectations of the future constantly change based on updated evidence and affect the dynamic allocation of attention. To further investigate the neural mechanisms underlying attentional expectancies, we employed a modified Central Cue Posner Paradigm in which the probability of cues being valid (that is, accurately indicated the upcoming target location) was manipulated. Attentional deployment to the cued location (α), which was governed by precision of predictions on previous trials, was estimated using a hierarchical Bayesian model and was included as a regressor in the analyses of electrophysiological (EEG) data. Our results revealed that before the target appeared, alpha oscillations (8∼13 Hz) for high-predictability cues (88 % valid) were significantly predicted by precision-dependent attention (α). This relationship was not observed under low-predictability conditions (69 % and 50 % valid cues). After the target appeared, precision-dependent attention (α) correlated with alpha band oscillations only in the valid cue condition and not in the invalid condition. Further analysis under conditions of significant attentional modulation by precision suggested a separate effect of cue orientation. These results provide new insights on how trial-by-trial Bayesian belief updating relates to alpha band encoding of environmentally-sensitive allocation of visual spatial attention.

The neural substrates of how model-based learning affects risk taking: Functional coupling between right cerebellum and left caudate.

Higher executive control capacity allows people to appropriately evaluate risk and avoid both excessive risk aversion and excessive risk-taking. The neural mechanisms underlying this relationship between executive function and risk taking are still unknown. We used voxel-based morphometry (VBM) analysis combined with resting-state functional connectivity (rs-FC) to evaluate how one component of executive function, model-based learning, relates to risk taking. We measured individuals' use of the model-based learning system with the two-step task, and risk taking with the Balloon Analogue Risk Task. Behavioral results indicated that risk taking was positively correlated with the model-based weighting parameter ω. The VBM results showed a positive association between model-based learning and gray matter volume in the right cerebellum (RCere) and left inferior parietal lobule (LIPL). Functional connectivity results suggested that the coupling between RCere and the left caudate (LCAU) was correlated with both model-based learning and risk taking. Mediation analysis indicated that RCere-LCAU functional connectivity completely mediated the effect of model-based learning on risk taking. These results indicate that learners who favor model-based strategies also engage in more appropriate risky behaviors through interactions between reward-based learning, error-based learning and executive control subserved by a caudate, cerebellar and parietal network.

Electrophysiological Signatures of Hierarchical Learning.

Human perception and learning is thought to rely on a hierarchical generative model that is continuously updated via precision-weighted prediction errors (pwPEs). However, the neural basis of such cognitive process and how it unfolds during decision-making remain poorly understood. To investigate this question, we combined a hierarchical Bayesian model (i.e., Hierarchical Gaussian Filter [HGF]) with electroencephalography (EEG), while participants performed a probabilistic reversal learning task in alternatingly stable and volatile environments. Behaviorally, the HGF fitted significantly better than two control, nonhierarchical, models. Neurally, low-level and high-level pwPEs were independently encoded by the P300 component. Low-level pwPEs were reflected in the theta (4-8 Hz) frequency band, but high-level pwPEs were not. Furthermore, the expressions of high-level pwPEs were stronger for participants with better HGF fit. These results indicate that the brain employs hierarchical learning and encodes both low- and high-level learning signals separately and adaptively.

Dynamic integration and segregation of amygdala subregional functional circuits linking to physiological arousal.

The dynamical organization of brain networks is essential to support human cognition and emotion for rapid adaption to ever-changing environment. As the core nodes of emotion-related brain circuitry, the basolateral amygdala (BLA) and centromedial amygdala (CMA) as two major amygdalar nuclei, are recognized to play distinct roles in affective functions and internal states, via their unique connections with cortical and subcortical structures in rodents. However, little is known how the dynamical organization of emotion-related brain circuitry reflects internal autonomic responses in humans. Using resting-state functional magnetic resonance imaging (fMRI) with K-means clustering approach in a total of 79 young healthy individuals (cohort 1: 42; cohort 2: 37), we identified two distinct states of BLA- and CMA-based intrinsic connectivity patterns, with one state (integration) showing generally stronger BLA- and CMA-based intrinsic connectivity with multiple brain networks, while the other (segregation) exhibiting weaker yet dissociable connectivity patterns. In an independent cohort 2 of fMRI data with concurrent recording of skin conductance, we replicated two similar dynamic states and further found higher skin conductance level in the integration than segregation state. Moreover, machine learning-based Elastic-net regression analyses revealed that time-varying BLA and CMA intrinsic connectivity with distinct network configurations yield higher predictive values for spontaneous fluctuations of skin conductance level in the integration than segregation state. Our findings highlight dynamic functional organization of emotion-related amygdala nuclei circuits and networks and its links to spontaneous autonomic arousal in humans.

Frontostriatal Functional Connectivity Underlies the Association between Punishment Sensitivity and Procrastination.

Procrastination is defined as putting off an intended course of action voluntarily despite the harmful consequences. Previous studies have suggested that procrastination is associated with punishment sensitivity in that high punishment sensitivity results in increased negative utility for task performance. We hypothesized the effects of punishment sensitivity on procrastination would be mediated by a network connecting the caudate nucleus and prefrontal cortex, both of which have been previously associated with self-control and emotional control during procrastination. We employed voxel-based morphometry (VBM) and resting-state functional connectivity (rsFC) to examine the neural substrates of punishment sensitivity and its relationship with procrastination (N = 268). The behavioral results indicated a strong positive correlation between measures of punishment sensitivity and procrastination. The VBM analysis revealed that the gray matter (GM) volume of the right caudate was significantly positively correlated with punishment sensitivity. The primary rsFC analysis revealed connectivity between this caudate location and the bilateral middle frontal gyrus (MFG) was significantly negatively correlated with punishment sensitivity. A mediation model indicated punishment sensitivity completely mediated the relation between functional connectivity within a caudate-bilateral MFG network and procrastination. Our results support the theory that those with higher punishment sensitivity have weaker effective emotional self-control supported by the caudate-MFG network, resulting in greater procrastination.

The Neural Mechanism of Number Line Bisection: A fMRI study.

The neural networks involved in number line bisection are poorly understood. We used functional magnetic resonance imaging (fMRI) to investigate these. fMRI was analyzed from 28 healthy volunteers who performed number and physical line bisection tasks (and their respective baselines). Whole brain analyses showed that these two bisection tasks shared common neural correlates in bilateral parietal-frontal networks; furthermore, bilateral parietal-frontal areas, right cerebellum, left insula and supplementary motor area (SMA) showed higher activity when contrasting the number line with a physical line bisection task. Importantly, psychophysiological interaction (PPI) analyses further indicated that left SMA and right cerebellum were connected to parietal-frontal areas for implementing the number line bisection task. Our findings suggested that a visuospatial attention control system was recruited, and mental imagery of a number line was used to find the midpoint of a numerical interval without calculations.

The metaphoric nature of the ordinal position effect.

Serial orders are thought to be spatially represented in working memory: The beginning items in the memorised sequence are associated with the left side of space and the ending items are associated with the right side of space. However, the origin of this ordinal position effect has remained unclear. It was suggested that the direction of serial order-space interaction is related to the reading/writing experience. An alternative hypothesis is that it originates from the "more is right"/"more is up" spatial metaphors we use in daily life. We can adjudicate between the two viewpoints in Chinese readers; they read left-to-right but also have a culturally ancient top-to-bottom reading/writing direction. Thus, the reading/writing viewpoint predicts no or a top-to-bottom effect in serial order-space interaction; whereas the spatial metaphor theory predicts a clear bottom-to-top effect. We designed four experiments to investigate this issue. First, we found a left-to-right ordinal position effect, replicating results obtained in Western populations. However, the vertical ordinal position effect was in the bottom-to-top direction; moreover, it was modulated by hand position (e.g., left hand bottom or up). We suggest that order-space interactions may originate from different sources and are driven by metaphoric comprehension, which itself may ground cognitive processing.

Addition and Subtraction but Not Multiplication and Division Cause Shifts of Spatial Attention.

Many studies have shown that solving addition and subtraction problems can induce overt shifts of spatial attention. In particular, right-side targets are detected faster than left-side targets when preceded by an addition operation, while left-side targets are detected faster than right-side targets when preceded by a subtraction operation. However, the interaction between space and arithmetic in multiplication or division is hardly studied and remains controversial. In order to make a strong case for the interaction between space and mental arithmetic, we attempted to replicate the spatial-arithmetic association in addition and subtraction (Experiment 1), and at the same time investigated whether shift of spatial attention would also be induced by multiplication or division operations (Experiment 2). We found that solving addition problems facilitated the detection of right-side targets, whereas left-side targets were detected faster after solving subtraction problems. However, no interaction between space and arithmetic operation was observed in multiplication or division. The implication of these findings is discussed.