Interindividual aperiodic resting-state EEG activity predicts cognitive-control styles.

The ability to find the right balance between more persistent and more flexible cognitive-control styles is known as "metacontrol." Recent findings suggest a relevance of aperiodic EEG activity and task conditions that are likely to elicit a specific metacontrol style. Here we investigated whether individual differences in aperiodic EEG activity obtained off-task (during resting state) predict individual cognitive-control styles under task conditions that pose different demands on metacontrol. We analyzed EEG resting-state data, task-EEG, and behavioral outcomes from a sample of N = 65 healthy participants performing a Go/Nogo task. We examined aperiodic activity as indicator of "neural noise" in the EEG power spectrum, and participants were assigned to a high-noise or low-noise group according to a median split of the exponents obtained for resting state. We found that off-task aperiodic exponents predicted different cognitive-control styles in Go and Nogo conditions: Overall, aperiodic exponents were higher (i.e., noise was lower) in the low-noise group, who however showed no difference between Go and Nogo trials, whereas the high-noise group exhibited significant noise reduction in the more persistence-heavy Nogo condition. This suggests that trait-like biases determine the default cognitive-control style, which however can be overwritten or compensated for under challenging task demands. We suggest that aperiodic activity in EEG signals represents valid indicators of highly dynamic arbitration between metacontrol styles, representing the brain's capability to reorganize itself and adapt its neural activity patterns to changing environmental conditions.

The Ability to Voluntarily Regulate Theta Band Activity Affects How Pharmacological Manipulation of the Catecholaminergic System Impacts Cognitive Control.

BACKGROUND: The catecholaminergic system influences response inhibition, but the magnitude of the impact of catecholaminergic manipulation is heterogeneous. Theoretical considerations suggest that the voluntary modulability of theta band activity can explain this variance. The study aimed to investigate to what extent interindividual differences in catecholaminergic effects on response inhibition depend on voluntary theta band activity modulation. METHODS: A total of 67 healthy adults were tested in a randomized, double-blind, cross-over study design. At each appointment, they received a single dose of methylphenidate or placebo and performed a Go/Nogo task with stimuli of varying complexity. Before the first appointment, the individual's ability to modulate theta band activity was measured. Recorded EEG data were analyzed using temporal decomposition and multivariate pattern analysis. RESULTS: Methylphenidate effects and voluntary modulability of theta band activity showed an interactive effect on the false alarm rates of the different Nogo conditions. The multivariate pattern analysis revealed that methylphenidate effects interacted with voluntary modulability of theta band activity at a stimulus processing level, whereas during response selection methylphenidate effects interacted with the complexity of the Nogo condition. CONCLUSIONS: The findings reveal that the individual's theta band modulability affects the responsiveness of an individual's catecholaminergic system to pharmacological modulation. Thus, the impact of pharmacological manipulation of the catecholaminergic system on cognitive control most likely depends on the existing ability to self-modulate relevant brain oscillatory patterns underlying the cognitive processes being targeted by pharmacological modulations.

Alpha and theta band activity share information relevant to proactive and reactive control during conflict-modulated response inhibition.

Response inhibition is an important instance of cognitive control and can be complicated by perceptual conflict. The neurophysiological mechanisms underlying these processes are still not understood. Especially the relationship between neural processes directly preceding cognitive control (proactive control) and processes underlying cognitive control (reactive control) has not been examined although there should be close links. In the current study, we investigate these aspects in a sample of N = 50 healthy adults. Time-frequency and beamforming approaches were applied to analyze the interrelation of brain states before (pre-trial) and during (within-trial) cognitive control. The behavioral data replicate a perceptual conflict-dependent modulation of response inhibition. During the pre-trial period, insular, inferior frontal, superior temporal, and precentral alpha activity was positively correlated with theta activity in the same regions and the superior frontal gyrus. Additionally, participants with a stronger pre-trial alpha activity in the primary motor cortex showed a stronger (within-trial) conflict effect in the theta band in the primary motor cortex. This theta conflict effect was further related to a stronger theta conflict effect in the midcingulate cortex until the end of the trial. The temporal cascade of these processes suggests that successful proactive preparation (anticipatory information gating) entails a stronger reactive processing of the conflicting stimulus information likely resulting in a realization of the need to adapt the current action plan. The results indicate that theta and alpha band activity share and transfer aspects of information when it comes to the interrelationship between proactive and reactive control during conflict-modulated motor inhibition.

Auricular Transcutaneous Vagus Nerve Stimulation Specifically Enhances Working Memory Gate Closing Mechanism: A System Neurophysiological Study.

Everyday tasks and goal-directed behavior involve the maintenance and continuous updating of information in working memory (WM). WM gating reflects switches between these two core states. Neurobiological considerations suggest that the catecholaminergic and the GABAergic are likely involved in these dynamics. Both of these neurotransmitter systems likely underlie the effects to auricular transcutaneous vagus nerve stimulation (atVNS). We examine the effects of atVNS on WM gating dynamics and their underlying neurophysiological and neurobiological processes in a randomized crossover study design in healthy humans of both sexes. We show that atVNS specifically modulates WM gate closing and thus specifically modulates neural mechanisms enabling the maintenance of information in WM. WM gate opening processes were not affected. atVNS modulates WM gate closing processes through the modulation of EEG alpha band activity. This was the case for clusters of activity in the EEG signal referring to stimulus information, motor response information, and fractions of information carrying stimulus-response mapping rules during WM gate closing. EEG-beamforming shows that modulations of activity in fronto-polar, orbital, and inferior parietal regions are associated with these effects. The data suggest that these effects are not because of modulations of the catecholaminergic (noradrenaline) system as indicated by lack of modulatory effects in pupil diameter dynamics, in the inter-relation of EEG and pupil diameter dynamics and saliva markers of noradrenaline activity. Considering other findings, it appears that a central effect of atVNS during cognitive processing refers to the stabilization of information in neural circuits, putatively mediated via the GABAergic system.SIGNIFICANCE STATEMENT Goal-directed behavior depends on how well information in short-term memory can be flexibly updated but also on how well it can be shielded from distraction. These two functions were guarded by a working memory gate. We show how an increasingly popular brain stimulation techniques specifically enhances the ability to close the working memory gate to shield information from distraction. We show what physiological and anatomic aspects underlie these effects.

Deep learning on independent spatial EEG activity patterns delineates time windows relevant for response inhibition.

Inhibitory control processes are an important aspect of executive functions and goal-directed behavior. However, the mostly correlative nature of neurophysiological studies was not able to provide insights which aspects of neural dynamics can best predict whether an individual is confronted with a situation requiring the inhibition of a response. This is particularly the case when considering the complex spatio-temporal nature of neural processes captured by EEG data. In the current study, we ask whether independent spatial activity profiles in the EEG data are useful to predict whether an individual is confronted with a situation requiring response inhibition. We combine independent component analysis (ICA) with explainable artificial intelligence approaches (EEG-based deep learning) using data from a Go/Nogo task (N = 255 participants). We show that there are four dissociable spatial activity profiles important to classify Go and Nogo trials as revealed by deep learning. Of note, for all of these four independent activity profiles, neural activity in the time period between 300 and 550 ms after stimulus presentation was most informative. Source localization analyses further revealed regions in the pre-central gyrus (BA6), the middle frontal gyrus (BA10), the inferior frontal gyrus (BA46), and the insular cortex (BA13) were associated with the isolated spatial activity profiles. The data suggest concomitant processes being reflected in the identified time window. This has implications for the ongoing debate on the functional significance of event-related potential correlates of inhibitory control.

Unsigned surprise but not reward magnitude modulates the integration of motor elements during actions.

It seems natural that motor responses unfold smoothly and that we are able to easily concatenate different components of movements to achieve goal-directed actions. Theoretical frameworks suggest that different motor features have to be bound to each other to achieve a coherent action. Yet, the nature of the "glue" (i.e., bindings) between elements constituting a motor sequence and enabling a smooth unfolding of motor acts is not well understood. We examined in how far motor feature bindings are affected by reward magnitude or the effects of an unsigned surprise signal. We show that the consistency of action file binding strength is modulated by unsigned surprise, but not by reward magnitude. On a conceptual and theoretical level, the results provide links between frameworks, which have until now not been brought into connection. In particular, theoretical accounts stating that only the unexpectedness (surprisingness) is essential for action control are connected to meta-control accounts of human action control.

Aperiodic neural activity reflects metacontrol.

Higher-level cognitive functions are mediated via complex oscillatory activity patterns and its analysis is dominating cognitive neuroscience research. However, besides oscillatory (period) activity, also aperiodic activity constitutes neural dynamics, but its relevance for higher-level cognitive functions is only beginning to be understood. The present study examined whether the broadband EEG aperiodic activity reflects principles of metacontrol. Metacontrol conceptualizes whether it is more useful to engage in more flexible processing of incoming information or to shield cognitive processes from incoming information (persistence-heavy processing). We examined EEG and behavioral data from a sample of n = 191 healthy participants performing a Simon Go/NoGo task that can be assumed to induce different metacontrol states (persistence-biased vs. flexibility-biased). Aperiodic activity was estimated using the FOOOF toolbox in the EEG power spectrum. There was a higher aperiodic exponent and offset in NoGo trials compared with Go trials, in incongruent (Go) trials compared with congruent (Go) trials. Thus, aperiodic activity increases during persistence-heavy processing, but decreases during flexibility-heavy processing. These findings link aperiodic features of the EEG signal and concepts describing the dynamics of how cognitive control modes are applied. Therefore, the study substantially extends the importance of aperiodic activity in understanding cognitive functions.

The role of visual association cortices during response selection processes in interference-modulated response stopping.

Response inhibition and the ability to navigate distracting information are both integral parts of cognitive control and are imperative to adaptive behavior in everyday life. Thus far, research has only inconclusively been able to draw inferences regarding the association between response stopping and the effects of interfering information. Using a novel combination of the Simon task and a stop signal task, the current study set out to investigate the behavioral as well as the neurophysiological underpinnings of the relationship between response stopping and interference processing. We tested n = 27 healthy individuals and combined temporal EEG signal decomposition with source localization methods to delineate the precise neurophysiological dynamics and functional neuroanatomical structures associated with conflict effects on response stopping. The results showed that stopping performance was compromised by conflicts. Importantly, these behavioral effects were reflected by specific aspects of information coded in the neurophysiological signal, indicating that conflict effects during response stopping are not mediated via purely perceptual processes. Rather, it is the processing of specific, stop-relevant stimulus features in the sensory regions during response selection, which underlies the emergence of conflict effects in response stopping. The findings connect research regarding response stopping with overarching theoretical frameworks of perception-action integration.

The neural stability of perception-motor representations affects action outcomes and behavioral adaptation.

Actions can fail - even though this is well known, little is known about what distinguishes neurophysiological processes preceding errors and correct actions. In this study, relying on the Theory of Event Coding, we test the assumption that only specific aspects of information coded in EEG activity are relevant for understanding processes leading to response errors. We examined N = 69 healthy participants who performed a mental rotation task and combined temporal EEG signal decomposition with multivariate pattern analysis (MVPA) and source localization analyses. We show that fractions of the EEG signal, primarily representing stimulus-response translation (event file) processes and motor response representations, are essential. Stimulus representations were less critical. The source localization results revealed widespread activity modulations in structures including the frontopolar, the middle and superior frontal, the anterior cingulate cortex, the cuneus, the inferior parietal cortex, and the ventral stream regions. These are associated with differential effects of the neural dynamics preceding correct/erroneous responses. The temporal-generalization MVPA showed that event file representations and representations of the motor response were already distinct 200 ms after stimulus presentation and this lasted till around 700 ms. The stability of this representational content was predictive for the magnitude of posterror slowing, which was particularly strong when there was no clear distinction between the neural activity profile of event file representations associated with a correct or an erroneous response. The study provides a detailed analysis of the dynamics leading to an error/correct response in connection to an overarching framework on action control.

Perception-action integration during inhibitory control is reflected in a concomitant multi-region processing of specific codes in the neurophysiological signal.

The integration of perception and action has long been studied in psychological science using overarching cognitive frameworks. Despite these being very successful in explaining perception-action integration, little is known about its neurophysiological and especially the functional neuroanatomical foundations. It is unknown whether distinct brain structures are simultaneously involved in the processing of perception-action integration codes and also to what extent demands on perception-action integration modulate activities in these structures. We investigate these questions in an EEG study integrating temporal and ICA-based EEG signal decomposition with source localization. For this purpose, we used data from 32 healthy participants who performed a 'TEC Go/Nogo' task. We show that the EEG signal can be decomposed into components carrying different informational aspects or processing codes relevant for perception-action integration. Importantly, these specific codes are processed independently in different brain structures, and their specific roles during the processing of perception-action integration differ. Some regions (i.e., the anterior cingulate and insular cortex) take a 'default role' because these are not modulated in their activity by demands or the complexity of event file coding processes. In contrast, regions in the motor cortex, middle frontal, temporal, and superior parietal cortices were not activated by 'default' but revealed modulations depending on the complexity of perception-action integration (i.e., whether an event file has to be reconfigured). Perception-action integration thus reflects a multi-region processing of specific fractions of information in the neurophysiological signal. This needs to be taken into account when further developing a cognitive science framework detailing perception-action integration.

Evidence for independent representational contents in inhibitory control subprocesses associated with frontoparietal cortices.

Inhibitory control processes have intensively been studied in cognitive science for the past decades. Even though the neural dynamics underlying these processes are increasingly better understood, a critical open question is how the representational dynamics of the inhibitory control processes are modulated when engaging in response inhibition in a relatively automatic or a controlled mode. Against the background of an overarching theory of perception-action integration, we combine temporal and spatial EEG signal decomposition methods with multivariate pattern analysis and source localization to obtain fine-grained insights into the neural dynamics of the representational content of response inhibition. For this purpose, we used a sample of N = 40 healthy adult participants. The behavioural data suggest that response inhibition was better in a more controlled than a more automated response execution mode. Regarding neural dynamics, effects of response inhibition modes relied on a concomitant coding of stimulus-related information and rules of how stimulus information is related to the appropriate motor programme. Crucially, these fractions of information, which are encoded at the same time in the neurophysiological signal, are based on two independent spatial neurophysiological activity patterns, also showing differences in the temporal stability of the representational content. Source localizations revealed that the precuneus and inferior parietal cortex regions are more relevant than prefrontal areas for the representation of stimulus-response selection codes. We provide a blueprint how a concatenation of EEG signal analysis methods, capturing distinct aspects of neural dynamics, can be connected to cognitive science theory on the importance of representations in action control.

Cognitive science theory-driven pharmacology elucidates the neurobiological basis of perception-motor integration.

An efficient integration of sensory and motor processes is crucial to goal-directed behavior. Despite this high relevance, and although cognitive theories provide clear conceptual frameworks, the neurobiological basis of these processes remains insufficiently understood. In a double-blind, randomized placebo-controlled pharmacological study, we examine the relevance of catecholamines for perception-motor integration processes. Using EEG data, we perform an in-depth analysis of the underlying neurophysiological mechanisms, focusing on sensorimotor integration processes during response inhibition. We show that the catecholaminergic system affects sensorimotor integration during response inhibition by modulating the stability of the representational content. Importantly, catecholamine levels do not affect the stability of all aspects of information processing during sensorimotor integration, but rather-as suggested by cognitive theory-of specific codes in the neurophysiological signal. Particularly fronto-parietal cortical regions are associated with the identified mechanisms. The study shows how cognitive science theory-driven pharmacology can shed light on the neurobiological basis of perception-motor integration and how catecholamines affect specific information codes relevant to cognitive control.

Processing of embedded response plans is modulated by an interplay of frontoparietal theta and beta activity.

Even simple actions like opening a door require integration/binding and flexible reactivation of different motor elements. Yet, the neural mechanisms underlying the processing of such "embedded response plans" are largely elusive, despite theoretical frameworks, such as the theory of event coding, describing the involved cognitive processes. In a sample of n = 40 healthy participants, we combine time-frequency decomposition and various beamforming methods to examine the neurophysiological dynamics of such action plans, with special emphasis on the interplay of theta and beta frequency activity during the processing of these plans. We show that the integration and rule-guided reactivation of embedded response plans is modulated by a complex interplay of theta and beta activity. Pretrial beta-band activity (BBA) is related to different functional neuroanatomical structures that are activated in a consecutive fashion. Enhanced preparatory activity is positively associated with higher binding-related BBA in the precuneus/parietal areas, indicating that activity in the precuneus/parietal cortex facilitates the execution of an embedded action sequence. Increased preparation subsequently leads to reduced working memory retrieval demands. A cascading pattern of interactions between pretrial and within-trial activity indicates the importance of preparatory brain activity. The study shows that there are multiple roles of beta and theta oscillations associated with different functional neuroanatomical structures during the integration and reactivation of motor elements during actions.NEW & NOTEWORTHY Even simple actions like opening a door require integration/binding and flexible reactivation of different motor elements. Yet, the neural mechanisms underlying the processing of such "embedded response plans" are largely elusive. The study shows that there are multiple roles of beta and theta oscillations associated with different functional neuroanatomical structures during the integration and reactivation of motor elements during actions.

Protocol to decode representations from EEG data with intermixed signals using temporal signal decomposition and multivariate pattern-analysis.

The electroencephalogram (EEG) is one of the most widely used techniques in cognitive neuroscience. We present a protocol showing how to combine a temporal signal decomposition approach (RIDE, Residue iteration decomposition) with multivariate pattern analysis (MVPA) to obtain insights into the temporal stability of representations coded in distinct informational fractions of the EEG signal. In this protocol, we describe pre-processing of human EEG data, followed by the set-up and use of MATLAB-based toolboxes for RIDE and MVPA analysis. For complete details on the use and execution of this protocol, please refer to Petruo et al. (2021).

Resting-state theta activity is linked to information content-specific coding levels during response inhibition.

The neurophysiological processes underlying the inhibition of impulsive responses have been studied extensively. While also the role of theta oscillations during response inhibition is well examined, the relevance of resting-state theta activity for inhibitory control processes is largely unknown. We test the hypothesis that there are specific relationships between resting-state theta activity and sensory/motor coding levels during response inhibition using EEG methods. We show that resting theta activity is specifically linked to the stimulus-related fraction of neurophysiological activity in specific time windows during motor inhibition. In contrast, concomitantly coded processes related to decision-making or response selection as well as the behavioral inhibition performance were not associated with resting theta activity. Even at the peak of task-related theta power, where task-related theta activity and resting theta activity differed the most, there was still predominantly a significant correlation between both types of theta activity. This suggests that aspects similar to resting dynamics are evident in the proportion of inhibition-related neurophysiological activity that reflects an "alarm" signal, whose function is to process and indicate the need for cognitive control. Thus, specific aspects of task-related theta power may build upon resting theta activity when cognitive control is necessary.

Alpha and Theta Bands Dynamics Serve Distinct Functions during Perception-Action Integration in Response Inhibition.

The ability to inhibit responses is central for situational behavior. However, the mechanisms how sensory information is used to inform inhibitory control processes are incompletely understood. In the current study, we examined neurophysiological processes of perception-action integration in response inhibition using the theory of event coding as a conceptual framework. Based on theoretical considerations, we focused on theta and alpha band activity in close connection to the functional neuroanatomical level using EEG beamforming. Moreover, we performed a network-based analysis of theta and alpha band activity. We show a seesaw-like relationship between medial and superior frontal cortex theta band activity and frontoparietal cortex alpha band activity during perception-action integration in response inhibition, depending on the necessity to reconfigure perception-action associations. When perception-action integration was more demanding, because perception-action associations (bindings) have to be reconfigured, there was an increase of theta and a decrease of alpha band activity. Vice versa, when there was no need to reconfigure perception-action bindings, theta band activity was low and alpha band activity was high. However, theta band processes seem to be most important for perception-action integration in response inhibition, because only the sensor-level network organization of theta band activity showed variations depending on the necessity to reconfigure perception-action associations. When no reconfiguration was necessary, the network architecture was more small-world-like, likely enabling efficient processing. When reconfigurations were necessary, the network organization becomes more random. These differences were particularly strong for fractions of the neurophysiological signal supposed to reflect response selection processes.

Auricular Transcutaneous Vagus Nerve Stimulation Diminishes Alpha-Band-Related Inhibitory Gating Processes During Conflict Monitoring in Frontal Cortices.

BACKGROUND: Pursuing goals is compromised when being confronted with interfering information. In such situations, conflict monitoring is important. Theoretical considerations on the neurobiology of response selection and control suggest that auricular transcutaneous vagus nerve stimulation (atVNS) should modulate conflict monitoring. However, the neurophysiological-functional neuroanatomical underpinnings are still not understood. METHODS: AtVNS was applied in a randomized crossover study design (n = 45). During atVNS or sham stimulation, conflict monitoring was assessed using a Flanker task. EEG data were recorded and analyzed with focus on theta and alpha band activity. Beamforming was applied to examine functional neuroanatomical correlates of atVNS-induced EEG modulations. Moreover, temporal EEG signal decomposition was applied to examine different coding levels in alpha and theta band activity. RESULTS: AtVNS compromised conflict monitoring processes when it was applied at the second appointment in the crossover study design. On a neurophysiological level, atVNS exerted specific effects because only alpha-band activity was modulated. Alpha-band activity was lower in middle and superior prefrontal regions during atVNS stimulation and thus lower when there was also a decline in task performance. The same direction of alpha-band modulations was evident in fractions of the alpha-band activity coding stimulus-related processes, stimulus-response translation processes, and motor response-related processes. CONCLUSIONS: The combination of prior task experience and atVNS compromises conflict monitoring processes. This is likely due to reduction of the alpha-band-associated inhibitory gating process on interfering information in frontal cortices. Future research should pay considerable attention to boundary conditions affecting the direction of atVNS effects.

Conditional generative adversarial networks applied to EEG data can inform about the inter-relation of antagonistic behaviors on a neural level.

Goal-directed actions frequently require a balance between antagonistic processes (e.g., executing and inhibiting a response), often showing an interdependency concerning what constitutes goal-directed behavior. While an inter-dependency of antagonistic actions is well described at a behavioral level, a possible inter-dependency of underlying processes at a neuronal level is still enigmatic. However, if there is an interdependency, it should be possible to predict the neurophysiological processes underlying inhibitory control based on the neural processes underlying speeded automatic responses. Based on that rationale, we applied artificial intelligence and source localization methods to human EEG recordings from N = 255 participants undergoing a response inhibition experiment (Go/Nogo task). We show that the amplitude and timing of scalp potentials and their functional neuroanatomical sources during inhibitory control can be inferred by conditional generative adversarial networks (cGANs) using neurophysiological data recorded during response execution. We provide insights into possible limitations in the use of cGANs to delineate the interdependency of antagonistic actions on a neurophysiological level. Nevertheless, artificial intelligence methods can provide information about interdependencies between opposing cognitive processes on a neurophysiological level with relevance for cognitive theory.

Time-On-Task Effects on Working Memory Gating Processes-A Role of Theta Synchronization and the Norepinephrine System.

Performance impairment as an effect of prolonged engagement in a specific task is commonly observed. Although this is a well-known effect in everyday life, little is known about how this affects central cognitive functions such as working memory (WM) processes. In the current study, we ask how time-on-task affects WM gating processes and thus processes regulating WM maintenance and updating. To this end, we combined electroencephalography methods and recordings of the pupil diameter as an indirect of the norepinephrine (NE) system activity. Our results showed that only WM gate opening but not closing processes showed time-on-task effects. On the neurophysiological level, this was associated with modulation of dorsolateral prefrontal theta band synchronization processes, which vanished with time-on-task during WM gate opening. Interestingly, also the modulatory pattern of the NE system, as inferred using pupil diameter data, changed. At the beginning, a strong correlation of pupil diameter data and theta band synchronization processes during WM gate opening is observed. This modulatory effect vanished at the end of the experiment. The results show that time-on-task has very specific effects on WM gate opening and closing processes and suggests an important role of NE system in the time-on-task effect on WM gate opening process.