Joram van Driel

Not All Errors Are Alike: Theta and Alpha EEG Dynamics Relate to Differences in Error-Processing Dynamics

Performance errors in conflict tasks often result from inappropriate action impulses, and are thought to signal the need for increased control over the motor system. However, errors may also result from lapses in sustained attention, which may require different monitoring and adaptation mechanisms. Distinguishing between the mechanisms of adaptation is important as both error types may occur intermixed. To this end, we measured EEG of healthy human subjects while they performed three variants of the Simon task in which errors were more likely to occur due to attentional lapses, failures of motor control, or both. Behavioral results showed that subjects exhibited less conflict effects and less impulsive errors in sustained attention compared with the other Simon conditions. Time-frequency analyses of EEG data showed that the sustained attention Simon condition, compared with the motor control Simon condition, was characterized by: (1) less error-related MFC theta (4–8 Hz) power and an absence of error-related MFC–DLPFC theta phase synchronization; (2) stronger error-related suppression of parieto-occipital alpha (8–12 Hz) power and stronger parieto-occipital–frontal alpha synchronization. A control experiment, using SART (the Sustained Attention to Response Test), confirmed that adaptation after attentional lapses involved posterior alpha power suppression, in addition to inter-regional frontal theta activity. Together, these results suggest that at least two cortical mechanisms exist for performance monitoring, and that different tasks and task-settings can recruit these mechanisms in a different way. Post-error brain dynamics thus consist of heterogeneous activity from multiple neurocognitive processes.

Interregional alpha-band synchrony supports temporal cross-modal integration

In a continuously changing environment, time is a key property that tells us whether information from the different senses belongs together. Yet, little is known about how the brain integrates temporal information across sensory modalities. Using high-density EEG combined with a novel psychometric timing task in which human subjects evaluated durations of audiovisual stimuli, we show that the strength of alpha-band (8-12 Hz) phase synchrony between localizer-defined auditory and visual regions depended on cross-modal attention: during encoding of a constant 500 ms standard interval, audiovisual alpha synchrony decreased when subjects attended audition while ignoring vision, compared to when they attended both modalities. In addition, alpha connectivity during a variable target interval predicted the degree to which auditory stimulus duration biased time estimation while attending vision. This cross-modal interference effect was estimated using a hierarchical Bayesian model of a psychometric function that also provided an estimate of each individuals tendency to exhibit attention lapses. This lapse rate, in turn, was predicted by single-trial estimates of the stability of interregional alpha synchrony: when attending to both modalities, trials with greater stability in patterns of connectivity were characterized by reduced contamination by lapses. Together, these results provide new insights into a functional role of the coupling of alpha phase dynamics between sensory cortices in integrating cross-modal information over time.

(No) time for control: Frontal theta dynamics reveal the cost of temporally guided conflict anticipation

During situations of response conflict, cognitive control is characterized by prefrontal theta-band (3- to 8-Hz) activity. It has been shown that cognitive control can be triggered proactively by contextual cues that predict conflict. Here, we investigated whether a pretrial preparation interval could serve as such a cue. This would show that the temporal contingencies embedded in the task can be used to anticipate upcoming conflict. To this end, we recorded electroencephalography (EEG) from 30 human subjects while they performed a version of a Simon task in which the duration of a fixation cross between trials predicted whether the next trial would contain response conflict. Both their behavior and EEG activity showed a consistent but unexpected pattern of results: The conflict effect (increased reaction times and decreased accuracy on conflict as compared to nonconflict trials) was stronger when conflict was cued, and this was associated with stronger conflict-related midfrontal theta activity and functional connectivity. Interestingly, intervals that predicted conflict did show a pretarget increase in midfrontal theta power. These findings suggest that temporally guided expectations of conflict do heighten conflict anticipation, but also lead to less efficiently applied reactive control. We further explored this post-hoc interpretation by means of three behavioral follow-up experiments, in which we used nontemporal cues, semantically informative cues, and neutral cues. Together, this body of results suggests that the counterintuitive cost of conflict cueing may not be uniquely related to the temporal domain, but may instead be related to the implicitness and validity of the cue.

Temporal auditory processing at 17 months of age is associated with preliterate language comprehension and later word reading fluency: an ERP study

Dyslexia is heritable and associated with auditory processing deficits. We investigate whether temporal auditory processing is compromised in young children at-risk for dyslexia and whether it is associated with later language and reading skills. We recorded EEG from 17 months-old children with or without familial risk for dyslexia to investigate whether their auditory system was able to detect a temporal change in a tone pattern. The children were followed longitudinally and performed an intelligence- and language development test at ages 4 and 4.5 years. Literacy related skills were measured at the beginning of second grade, and word- and pseudo-word reading fluency were measured at the end of second grade. The EEG responses showed that control children could detect the temporal change as indicated by a mismatch response (MMR). The MMR was not observed in at-risk children. Furthermore, the fronto-central MMR amplitude correlated with preliterate language comprehension and with later word reading fluency, but not with phonological awareness. We conclude that temporal auditory processing differentiates young children at risk for dyslexia from controls and is a precursor of preliterate language comprehension and reading fluency.

Slow oscillations during sleep coordinate interregional communication in cortical networks

Large-amplitude sleep slow oscillations group faster neuronal oscillations and are of functional relevance for memory performance. However, relatively little is known about the impact of slow oscillations on functionally coupled networks. Here, we provide a comprehensive view on how human slow oscillatory dynamics influence various measures of brain processing. We demonstrate that slow oscillations coordinate interregional cortical communication, as assessed by phase synchrony in the sleep spindle frequency range and cross-frequency coupling between spindle and beta activity. Furthermore, we show that the organizing role of slow oscillations is restricted to circumscribed topographical areas. These findings add importantly to our basic understanding of the orchestrating role of slow oscillations. In addition, they are of considerable relevance for accounts of sleep-dependent memory reprocessing and consolidation.

Frequency Band-Specific Electrical Brain Stimulation Modulates Cognitive Control Processes

A large body of findings has tied midfrontal theta-band (4–8 Hz) oscillatory activity to adaptive control mechanisms during response conflict. Thus far, this evidence has been correlational. To evaluate whether theta oscillations are causally involved in conflict processing, we applied transcranial alternating current stimulation (tACS) in the theta band to a midfrontal scalp region, while human subjects performed a spatial response conflict task. Conflict was introduced by incongruency between the location of the target stimulus and the required response hand. As a control condition, we used alpha-band (8–12 Hz) tACS over the same location. The exact stimulation frequencies were determined empirically for each subject based on a pre-stimulation EEG session. Behavioral results showed general conflict effects of slower response times (RT) and lower accuracy for high conflict trials compared to low conflict trials. Importantly, this conflict effect was reduced specifically during theta tACS, which was driven by slower response times on low conflict trials. These results show how theta tACS can modulate adaptive cognitive control processes, which is in accordance with the view of midfrontal theta oscillations as an active mechanism for cognitive control.

Posterior α EEG Dynamics Dissociate Current from Future Goals in Working Memory-Guided Visual Search

Current models of visual search assume that search is guided by an active visual working memory representation of what we are currently looking for. This attentional template for currently relevant stimuli can be dissociated from accessory memory representations that are only needed prospectively, for a future task, and that should be prevented from guiding current attention. However, it remains unclear what electrophysiological mechanisms dissociate currently relevant (serving upcoming selection) from prospectively relevant memories (serving future selection). We measured EEG of 20 human subjects while they performed two consecutive visual search tasks. Before the search tasks, a cue instructed observers which item to look for first (current template) and which second (prospective template). During the delay leading up to the first search display, we found clear suppression of α band (8–14 Hz) activity in regions contralateral to remembered items, comprising both local power and interregional phase synchronization within a posterior parietal network. Importantly, these lateralization effects were stronger when the memory item was currently relevant (i.e., for the first search) compared with when it was prospectively relevant (i.e., for the second search), consistent with current templates being prioritized over future templates. In contrast, event-related potential analysis revealed that the contralateral delay activity was similar for all conditions, suggesting no difference in storage. Together, these findings support the idea that posterior α oscillations represent a state of increased processing or excitability in task-relevant cortical regions, and reflect enhanced cortical prioritization of memory representations that serve as a current selection filter. SIGNIFICANCE STATEMENT Our days are filled with looking for relevant objects while ignoring irrelevant visual information. Such visual search activity is thought to be driven by current goals activated in working memory. However, working memory not only serves current goals, but also future goals, with differential impact upon visual selection. Little is known about how the brain differentiates between current and future goals. Here we show, for the first time, that modulations of brain oscillations in the EEG α frequency band in posterior cortex can dissociate current from future search goals in working memory. Moreover, the dynamics of these oscillations uncover how we flexibly switch focus between memory representations. Together, we reveal how the brain assigns priority for selection.

Local and interregional alpha EEG dynamics dissociate between memory for search and memory for recognition

ABSTRACT Attention during visual search is thought to be guided by an active visual working memory (VWM) representation of the search target. We tested the hypothesis that a VWM representation used for searching a target among competing information (a “search template”) is distinct from VWM representations used for simple recognition tasks, without competition. We analyzed EEG from 20 human participants while they performed three different VWM‐based visual detection tasks. All tasks started with identical lateralized VWM cues, but differed with respect to the presence and nature of competing distractors during the target display at test, where participants performed a simple recognition task without distractors, or visual search in pop‐out (distinct) and serial (non‐distinct) search displays. Performance was worst for non‐distinct search, and best for simple recognition. During the one second delay period between cue and test, we observed robust suppression of EEG dynamics in the alpha (8–14 Hz) band over parieto‐occipital sites contralateral to the relevant VWM item, both in terms of local power as well as interregional phase synchrony within a posterior‐parietal network. Importantly, these lateralization dynamics were more strongly expressed prior to search compared to simple recognition. Furthermore, before the VWM cue, alpha phase synchrony between prefrontal and mid‐posterior‐parietal sites was strongest for non‐distinct search, reflecting enhanced anticipatory control prior to VWM encoding. Directional connectivity analyses confirmed this effect to be in an anterior‐to‐posterior direction. Together, these results provide evidence for frontally mediated top‐down control of VWM in preparation of visual search. HighlightsWe compared visual working memory prior to search versus simple recognition.Lateralized memoranda elicited robust contralateral alpha (8–14 Hz) suppression.Lateralized alpha suppression was stronger when memory was needed for visual search.Pre‐stimulus long‐range alpha connectivity was similarly modulated by task demands.We find that the alpha‐band supports increased top‐down control of search templates.

From ERPs to MVPA Using the Amsterdam Decoding and Modeling Toolbox (ADAM)

In recent years, time-resolved multivariate pattern analysis (MVPA) has gained much popularity in the analysis of electroencephalography (EEG) and magnetoencephalography (MEG) data. However, MVPA may appear daunting to those who have been applying traditional analyses using event-related potentials (ERPs) or event-related fields (ERFs). To ease this transition, we recently developed the Amsterdam Decoding and Modeling (ADAM) toolbox in MATLAB. ADAM is an entry-level toolbox that allows a direct comparison of ERP/ERF results to MVPA results using any dataset in standard EEGLAB or Fieldtrip format. The toolbox performs and visualizes multiple-comparison corrected group decoding and forward encoding results in a variety of ways, such as classifier performance across time, temporal generalization (time-by-time) matrices of classifier performance, channel tuning functions (CTFs) and topographical maps of (forward-transformed) classifier weights. All analyses can be performed directly on raw data or can be preceded by a time-frequency decomposition of the data in which case the analyses are performed separately on different frequency bands. The figures ADAM produces are publication-ready. In the current manuscript, we provide a cookbook in which we apply a decoding analysis to a publicly available MEG/EEG dataset involving the perception of famous, non-famous and scrambled faces. The manuscript covers the steps involved in single subject analysis and shows how to perform and visualize a subsequent group-level statistical analysis. The processing pipeline covers computation and visualization of group ERPs, ERP difference waves, as well as MVPA decoding results. It ends with a comparison of the differences and similarities between EEG and MEG decoding results. The manuscript has a level of description that allows application of these analyses to any dataset in EEGLAB or Fieldtrip format.

Beta and theta oscillations differentially support free versus forced control over target selection in visual search

Many important situations require human observers to simultaneously search for more than one object. Despite a long history of research into visual search, the behavioral and neural mechanisms associated with multiple-target search are poorly understood. Here we test the novel theory that the efficiency of looking for multiple targets critically depends on the mode of cognitive control the environment affords to the observer. We used an innovative combination of EEG and eye tracking while participants searched for two targets, within two different contexts: Either both targets were present in the search display and observers were free to prioritize either one of them, thus enabling proactive control over selection; or only one of the two targets would be present in each search display, which requires reactive control to reconfigure selection when the wrong target is prioritized. During proactive control, both univariate and multivariate signals of beta-band (15–35 Hz) power suppression prior to display onset predicted switches between target selections. This signal originated over midfrontal and sensorimotor regions and has previously been associated with endogenous state changes. In contrast, imposed target selections requiring reactive control elicited prefrontal power enhancements in the delta/theta-band (2–8 Hz), but only after display onset. This signal predicted individual differences in associated oculomotor switch costs, reflecting reactive reconfiguration of target selection. The results provide compelling evidence that multiple target representations are differentially prioritized during visual search, and for the first time reveal distinct neural mechanisms underlying proactive and reactive control over multiple-target search. Significance Statement Searching for more than one object in complex visual scenes can be detrimental for search performance. While perhaps annoying in daily life, this can have severe consequences in professional settings such as medical and security screening. Previous research has not yet resolved whether multiple-target search involves changing priorities in what people attend to, and how such changes are controlled. We approached these questions by concurrently measuring cortical activity and eye movements using EEG and eye tracking, while observers searched for multiple possible targets. Our findings provide the first unequivocal support for the existence of two modes of control during multiple-target search, which are expressed in qualitatively distinct time-frequency signatures of the EEG both before and after visual selection.