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

Abstract

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.

Two Independent Frontal Midline Theta Oscillations during Conflict Detection and Adaptation in a Simon-Type Manual Reaching Task

“…In the current study, we set out to explore whether there are several theta generators in or near anterior cingulate cortex that jointly give rise to the scalp-recorded EEG spectral responses typically found in paradigms involving S-R conflicts (Nigbur et al, 2011;Cavanagh et al, 2012;van Driel et al, 2012). In particular, we aimed at identifying the cortical areas generating conflictinduced fm complexes in a Simon-type manual reaching task to resolve the open issue whether multiple, conflict-related (detec- tion and adaptation) and conflict-unrelated processes (general RT slowing) can be linked to statistically independent fm oscillations; or, alternatively, whether multiple processes can drive one-and-the-same fm complex.…”

“…Complementing these hemodynamic findings, recent electroencephalographic (EEG) investigations have provided insights into the spectrotemporal brain dynamics that mediate conflict detection and adaptation in the classic Simon task (Cohen and Ridderinkhof, 2013;Gulbinaite et al, 2014) as well as in (cueing) variants of this task (Cavanagh et al, 2012;van Driel et al, 2015;Mückschel et al, 2016). The emerging picture suggests that the noncorrespondence between stimulus (S) and response (R) locations is associated with brief medial frontal cortex (MFC)-generated theta complexes.…”

Synchronizing theta oscillations with direct-current stimulation strengthens adaptive control in the human brain

“…Cluster analyses revealed significant Cz-seeded theta connectivity isolated to the frontolateral regions of the head (i.e., F3: 4.5-8 Hz, P = 0.004; F4-T4: 4-7.5 Hz, P = 0.009). Of note, our ability to capture the spatial specificity of this long-range theta effect was due, in part, to the Laplacian transform used to generate current-source density, which is known to highlight local electrical activity unique to each electrode while minimizing broadly distributed activity common to multiple electrodes (19,20,32) (Fig. 3B).…”

“…However, the functional significance of medial-frontal theta may be much broader than simply functioning as an alarm for the adaptive-control system. Theta oscillations have been hypothesized to serve as the temporal code that coordinates neuronal populations involved in implementing control (1,(19)(20)(21), with medial-frontal cortex working in concert with dorsolateral prefrontal areas to support flexible, adaptive behavior (1, 23-26). For example, when an error occurs, network-level oscillations allow executive mechanisms to adjust subordinate cognitive mechanisms (e.g., perceptual attention, response-selection thresholds).…”

“…The low-frequency oscillations are thought to reflect coordinated activity across the diverse set of brain areas recruited to perform a task (1,(17)(18)(19)(20)(21)(22). In addition, medial-frontal theta (4-8 Hz) oscillations appear to signal the need for adaptive control across a variety of tasks and situations.…”