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Verguts, T.

Publications and source records attributed to Verguts, T..

28 records · Page 2Linked to original sources

Theta and alpha power across fast and slow timescales in cognitive control

Theta and alpha frequency neural oscillations are important for learning and cognitive control, but their exact role has remained obscure. In particular, it is unknown whether they operate at similar timescales, and whether they support different cognitive processes. We recorded EEG in 30 healthy human participants while they performed a learning task containing both novel (block-unique) and repeating stimuli. We investigated behavior and electrophysiology at both fast (i.e., within blocks) and slow (i.e., between blocks) time scales. Behaviorally, both response time and accuracy improved (resp. decrease and increase) over both fast and slow timescales. However, on the spectral level, theta power significantly decreased along the slow timescale, whereas alpha power instead significantly increased along the fast timescale. We thus demonstrate that theta and alpha both play a role during learning, but operate at different timescales. This result poses important empirical constraints for theories on learning, cognitive control, and neural oscillations.

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Failure to modulate reward prediction errors in declarative learning with theta (6 Hz) frequency transcranial alternating current stimulation.

Recent evidence suggests that reward prediction errors (RPEs) play an important role in declarative learning, but its neurophysiological mechanism remains unclear. Here, we tested the hypothesis that RPEs modulate declarative learning via theta-frequency oscillations, which have been related to memory encoding in prior work. For that purpose, we examined the interaction between RPE and transcranial Alternating Current Stimulation (tACS) in declarative learning. Using a between-subject (real versus sham stimulation group), single-blind stimulation design, 76 participants learned 60 Dutch-Swahili word pairs, while theta-frequency (6 Hz) tACS was administered over the medial frontal cortex (MFC). Previous studies have implied MFC in memory encoding. We replicated our previous finding of signed RPEs (SRPEs) boosting declarative learning; with larger and more positive RPEs enhancing memory performance. However, tACS failed to modulate the SRPE effect in declarative learning and did not affect memory performance. Bayesian statistics supported evidence for an absence of effect. Our study confirms a role of RPE in declarative learning, but also calls for standardized procedures in transcranial electrical stimulation.

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Learning to synchronize: midfrontal theta dynamics during reversal learning

In recent years, several hierarchical extensions of well-known learning algorithms have been proposed. For example, when stimulus-action mappings vary across time or context, the brain may learn two or more stimulus-action mappings in separate modules, and additionally (at a hierarchically higher level) learn to appropriately switch between those modules. However, how the brain mechanistically coordinates neural communication to implement such hierarchical learning, remains unknown. Therefore, the current study tests a recent computational model that proposed how midfrontal theta oscillations implement such hierarchical learning via the principle of binding by synchrony (Sync model). More specifically, the Sync model employs bursts at theta frequency to flexibly bind appropriate task modules by synchrony. 64-channel EEG signal was recorded while 27 human subjects (Female: 21, Male: 6) performed a probabilistic reversal learning task. In line with the Sync model, post-feedback theta power showed a linear relationship with negative prediction errors, but not with positive prediction errors. This relationship was especially pronounced for subjects with better behavioral fit (measured via AIC) of the Sync model. Also consistent with Sync model simulations, theta phase-coupling between midfrontal electrodes and temporo-parietal electrodes was stronger after negative feedback. Our data suggest that the brain uses theta power and synchronization for flexibly switching between task rule modules, as is useful for example when multiple stimulus-action mappings must be retained and used. Significance StatementEveryday life requires flexibility in switching between several rules. A key question in understanding this ability is how the brain mechanistically coordinates such switches. The current study tests a recent computational framework (Sync model) that proposed how midfrontal theta oscillations coordinate activity in hierarchically lower task-related areas. In line with predictions of this Sync model, midfrontal theta power was stronger when rule switches were most likely (strong negative prediction error), especially in subjects who obtained a better model fit. Additionally, also theta phase connectivity between midfrontal and task-related areas was increased after negative feedback. Thus, the data provided support for the hypothesis that the brain uses theta power and synchronization for flexibly switching between rules.

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Dynamic expressions of confidence within an evidence accumulation framework

Human observers can reliably report their confidence in the choices they make. An influential framework conceptualizes decision confidence as the probability of a decision being correct, given the choice made and the evidence on which it was based. This framework accounts for three diagnostic signatures of human confidence reports, including an opposite dependence of confidence on evidence strength for correct and error trials. However, the framework does not account for the temporal evolution of these signatures, because it only describes the transformation of a static representation of evidence into choice and the associated confidence. Here, we combine this framework with another influential framework: dynamic accumulation of evidence over time, and build on the notion that confidence reflects the probability of being correct, given the choice and accumulated evidence up until that point. Critically, we show that such a dynamic model predicts that the diagnostic signatures of confidence depend on time; most critically, it predicts a stronger opposite dependence of confidence on evidence strength and choice correctness as a function of time. We tested, and confirmed, these predictions in human behaviour during random dot motion discrimination, in which confidence judgments were queried at different points in time. We conclude that human confidence reports reflect the dynamics of the probability of being correct given the accumulated evidence and choice.

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Signed Reward Prediction Errors in the Ventral Striatum Drive Episodic Memory

A growing body of behavioral evidence implicates reward prediction errors (RPEs) as a key factor in the acquisition of episodic memory. Yet, important neural predictions related to the role of RPE in declarative memory acquisition remain to be tested. Using a novel variable-choice task, we experimentally manipulated RPEs and found support for key predictions on the neural level with fMRI. Specifically, we demonstrate that trial-specific RPE responses in the ventral striatum (during learning) predict the strength of subsequent episodic memory (during recollection). Furthermore, functional connectivity between task-relevant processing areas (e.g., face-selective areas) and hippocampus, ventral tegmental area, and ventral striatum increased as a function of RPE value (during learning), suggesting a central role of these areas in episodic memory formation. Our results consolidate reinforcement learning theory and striatal RPEs as key operations subtending the formation of episodic memory.

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Post-decisional sense of confidence shapes speed-accuracy tradeoff for subsequent choices

When external feedback about decision outcomes is lacking, agents need to adapt their decision policies based on an internal estimate of the correctness of their choices (i.e., decision confidence). We hypothesized that agents use confidence to continuously update the tradeoff between the speed and accuracy of their decisions: When confidence is low in one decision, the agent needs more evidence before committing to a choice in the next decision, leading to slower but more accurate decisions. We tested this hypothesis by fitting a bounded accumulation decision model to behavioral data from three different perceptual choice tasks. Decision bounds indeed depended on the reported confidence on the previous trial, independent of objective accuracy. This increase in decision bound was predicted by a centro-parietal EEG component sensitive to confidence. We conclude that the brain uses internally computed confidence signals for the ongoing adjustment of decision policies.

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Learning to synchronize: How biological agents can couple neural task modules for dealing with the stability-plasticity dilemma

We provide a novel computational framework on how biological and artificial agents can learn to flexibly couple and decouple neural task modules for cognitive processing. In this way, they can address the stability-plasticity dilemma. For this purpose, we combine two prominent computational neuroscience principles, namely Binding by Synchrony and Reinforcement Learning. The model learns to synchronize task-relevant modules, while also learning to desynchronize currently task-irrelevant modules. As a result, old (but currently task-irrelevant) information is protected from overwriting (stability) while new information can be learned quickly in currently task-relevant modules (plasticity). We combine learning to synchronize with several classical learning algorithms (backpropagation, Boltzmann machines, Rescorla-Wagner). For each case, we demonstrate that our combined model has significant computational advantages over the original network in both stability and plasticity. Importantly, the resulting models processing dynamics are also consistent with empirical data and provide empirically testable hypotheses for future MEG/EEG studies.\n\nAuthor summaryArtificial and biological agents alike face a critical trade-off between being sufficiently adaptive to acquiring novel information (plasticity) and retaining older information (stability); this is known as the stability-plasticity dilemma. Previous work on this dilemma has focused either on computationally efficient solutions for artificial agents or on biologically plausible frameworks for biological agents. What is lacking is a solution that combines computational efficiency with biological plausibility. Therefore, the current work proposes a computational framework on the stability-plasticity dilemma that provides empirically testable hypotheses on both neural and behavioral levels. In this framework, neural task modules can be flexibly coupled and decoupled depending on the task at hand. Testing this framework will allow us to gain more insight in how biological agents deal with the stability-plasticity dilemma.

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A post-decisional neural marker of confidence predicts information-seeking

Theoretical work predicts that decisions made with low confidence should lead to increased information-seeking. This is an adaptive strategy because it can increase the quality of a decision, and previous behavioral work has shown that decision-makers engage in such confidence-driven information seeking. The present study aimed to characterize the neural markers that mediate the relationship between confidence and information-seeking. A paradigm was used in which human participants made an initial perceptual decision, and then decided whether or not they wanted to sample more evidence before committing to a final decision and confidence judgment. Pre-decisional and post-decisional ERP components were similarly modulated by the level of confidence and by information-seeking choices. Time-resolved multivariate decoding of scalp EEG signals first revealed that information-seeking choices could be decoded from the time of the initial decision to the time of the subsequent information-seeking choice (within-condition decoding). No above-chance decoding was visible in the pre-response time window. Crucially, a classifier trained to decode high versus low confidence predicted information-seeking choices after the initial perceptual decision (across-condition decoding). This time window corresponds to that of a post-decisional neural marker of confidence. Collectively, our findings demonstrate for the first time that neural indices of confidence are functionally involved in information-seeking decisions.

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Preparation for mental effort recruits Dorsolateral Prefrontal Cortex: an fNIRS investigation

Preparing for a mentally demanding task calls upon cognitive and motivational resources. The underlying neural implementation of these mechanisms is receiving growing attention, given the implications for professional, social, and medical contexts. While several fMRI studies converge in assigning a crucial role to a cortico-subcortical network including Anterior Cigulate Cortex (ACC) and striatum, the involvement of Dorsolateral Prefrontal Cortex (DLPFC) during mental effort anticipation has yet to be replicated. This study was designed to target DLPFC contribution using functional Near Infrared Spectroscopy (fNIRS), as a more cost-effective tool measuring cortical hemodynamics. We adapted a validated mental effort task, where participants performed easy and difficult mental calculation, while measuring DLPFC activity during the anticipation phase. As hypothesized, DLPFC activity increased during preparation for a hard task as compared to an easy task. Besides replicating a previous fMRI study, these results establish fNIRS as an effective tool to investigate cortical contributions to preparation for effortful behavior. This is especially useful if one requires testing large samples (e.g., to target individual differences), populations with contraindication for functional MRI (e.g., infants or patients with metal implants), or subjects in more naturalistic environments (e.g., work or sport).

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Dorsal Anterior Cingulate-Midbrain Ensemble As A Reinforcement Meta-Learner

The dorsal anterior cingulate cortex (dACC) is central in higher-order cognition and behavioural flexibility. The computational nature of this region, however, has remained elusive. Here we propose a new model - the Reinforcement Meta Learner (RML) - based on the bidirectional anatomical connections of the ACC with midbrain catecholamine nuclei (VTA and LC). In this circuit, dACC learns which actions are valuable and acts accordingly. Crucially, this mechanism is optimized by recurrent connectivity with the midbrain: Midbrain catecholamines provide modulatory signals to dACC, controlling its internal parameters (e.g. learning rate), while these parameter modulations are in turn optimized by dACC afferents to the midbrain. This closed-loop system generates emergent (i.e., homunculus-free) control and supports learning to solve hierarchical decision problems without having an intrinsic hierarchical structure itself. Further, it can be combined with other cortical modules to optimize the processing of these modules. We outline how the RML solves the current theoretical stalemate on dACC by assimilating various previous proposals on ACC functioning, and how it captures critical empirical findings from an unprecedented range of domains (stability/plasticity balance, effort processing, working memory, and higher-order classical and instrumental conditioning).

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