Frontal midline theta differentiates separate cognitive control strategies while still generalizing the need for cognitive control

Eisma, Jarrod; Rawls, Eric; Long, Stephanie; Mach, Russell; Lamm, Connie

doi:10.1038/s41598-021-94162-z

Cited by 39 publications

(31 citation statements)

References 59 publications

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“…We interpreted global increases in frontal-midline theta power as indicative of the higher need for cognitive control during memory suppression relative to voluntary retrieval, based on a well supported hypothesis about the role of this EEG marker ( Cavanagh and Frank, 2014 ). However, recent findings indicate that, although on average frontal-midline theta power is higher for conditions that require more cognitive control (here No-Think) relative to control conditions (e.g., Think), and correlate with slower behavior, increased frontal-midline theta power also indexes the extent to which control is engaged ( Eisma et al, 2021 ). Particularly, in trial-by-trial analyses focused within a condition, more theta predicts higher control engagement and faster responses on a task requiring inhibitory control ( Cooper et al, 2019 ).…”

Section: Resultsmentioning

confidence: 99%

Anterior Cingulate Cortex Signals the Need to Control Intrusive Thoughts during Motivated Forgetting

et al. 2022

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How do people limit awareness of unwanted memories? When such memories intrude, a control process engages the right DLPFC (rDLPFC) to inhibit hippocampal activity and stop retrieval. It remains unknown how the need for control is detected, and whether control operates proactively to prevent unwelcome memories from being retrieved, or responds reactively, to counteract intrusions. We hypothesized that dorsal ACC (dACC) detects the emergence of an unwanted trace in awareness and transmits the need for inhibitory control to rDLPFC. During a memory suppression task, we measured in humans (both sexes) trial-by-trial variations in the theta power and N2 amplitude of dACC, two EEG markers that are thought to reflect the need for control. With simultaneous EEG-fMRI recordings, we tracked interactions among dACC, rDLPFC, and hippocampus during suppression. We found a clear role of dACC in detecting the need for memory control and upregulating prefrontal inhibition. Importantly, we identified distinct early (300–450 ms) and late (500–700 ms) dACC contributions, suggesting both proactive control before recollection and reactive control in response to intrusions. Stronger early activity was associated with reduced hippocampal activity and diminished BOLD signal in dACC and rDLPFC, suggesting that preempting retrieval reduced overall control demands. In the later window, dACC activity was larger, and effective connectivity analyses revealed robust communication from dACC to rDLPFC and from rDLPFC to hippocampus, which are tied to successful forgetting. Together, our findings support a model in which dACC detects the emergence of unwanted content, triggering top-down inhibitory control, and in which rDLPFC countermands intruding thoughts that penetrate awareness. SIGNIFICANCE STATEMENT Preventing unwanted memories from coming to mind is an adaptive ability of humans. This ability relies on inhibitory control processes in the prefrontal cortex to modulate hippocampal retrieval processes. How and when reminders to unwelcome memories come to trigger prefrontal control mechanisms remains unknown. Here we acquired neuroimaging data with both high spatial and temporal resolution as participants suppressed specific memories. We found that the anterior cingulate cortex detects the need for memory control, responding both proactively to early warning signals about unwelcome content and reactively to intrusive thoughts themselves. When unwanted traces emerge in awareness, anterior cingulate communicates with prefrontal cortex and triggers top-down inhibitory control over the hippocampus through specific neural oscillatory networks.

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Section: Resultsmentioning

confidence: 99%

Anterior Cingulate Cortex Signals the Need to Control Intrusive Thoughts during Motivated Forgetting

et al. 2022

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“… 17 , 35 Jarrod et al Found that target conditions requiring more cognitive control elicited higher power theta activity in the frontal midline compared to control conditions. 36 Wang et al Used a two-choice Oddball task to study the behavioral inhibition of individuals at different altitudes, they found that theta power of deviant stimuli was significantly higher than that of standard stimuli, with individuals at higher altitudes requiring longer response times and electrophysiologically exhibiting lower P3 amplitude and theta power. 37 The results of the present study are consistent with this, with deviant stimuli triggering higher power theta bands in the frontal midline compared to standard stimuli.…”

Section: Discussionmentioning

confidence: 99%

Evoked Acute Stress Alters Frontal Midline Neural Oscillations Affecting Behavioral Inhibition in College Students

Wu¹,

Di²,

Ma³

2022

PRBM

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Purpose The current research of the effect of acute stress on individual behavioral inhibition remains divergent. The present study aims to explore the effects of acute stress on behavioral inhibition in college students and to understand the neural oscillatory characteristics of their behavioral inhibition process. Patients and Methods We invited 27 college students (12 males and 15 females) to participate in the study. The experiment was conducted using the Trier Social Stress paradigm to evoke an acute stress state and an out-of-speech reading to set a neutral state. Participants completed a two-choice Oddball task in the acute stress state and the neutral state, respectively. We used a 64-channel EEG cap to record EEG data from university students during the experimental task. In combination with the ERO technique, we compared the reaction time, the number of errors, and the power of the alpha (8–13 Hz) and theta (4–8 Hz) frequency bands at the midline of the frontal lobe for subjects in both states. The correlation between the area under the stress area line and the alpha as well as theta frequency bands was also analyzed. Results We found that in the two-choice Oddball task, the response inhibition time was shorter, the number of response errors decreased, and the alpha-band power values decreased in the acute stress state compared to the neutral state. For the standard stimulus, the theta-band power increase in the acute stress state. Conclusion Our results suggest that evoked acute stress promotes behavioral inhibition in college students by affecting their frontal midline neural oscillations.

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“…Somatomotor beta bursts, the motor inhibitory mechanism underlying PTSD-relevant cognitive control deficits, might also be under the control of executive brain regions via cross-frequency interactions (for example frontal midline theta). In healthy controls, but not individuals with PTSD, somatomotor beta activity was linked to prefrontal theta-band activation (Cohen et al, 2013) – a common substrate underlying multiple types of cognitive control (Cavanagh et al, 2012; Cavanagh & Frank, 2014; Eisma et al, 2021). Furthermore, in a sample of trauma-exposed veterans, increased cognitive control-related brain activation in the anterior cingulate cortex (ACC), a key brain region regulating cognitive control computations (Botvinick, 2007; Botvinick et al, 2004; Gehring & Knight, 2000; Sohn et al, 2007), was associated with reduced PTSD symptom severity (White et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Somatomotor Beta Bursts Mediate the Negative Impact of PTSD Severity on Conflict Monitoring

Rawls

Marquardt

Sponheim

2022

Preprint

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Cognitive control deficits are associated with posttraumatic stress disorder (PTSD) and may explain how reminders of past traumatic events intrude upon daily experiences of people who have experienced trauma. Lateralized somatomotor beta-band desynchronization, an electrophysiological signature of controlled movement, indexes the downstream output of cognitive control processes. Recent evidence suggests that somatomotor beta activity does not manifest as rhythmic oscillations, but instead as discrete and stochastic burst-like events. Here, we quantified the rates of lateralized somatomotor beta bursts (beta burst rates; BBR) evoked during a flanker cognitive control paradigm among United States military veterans from Operations Iraqi and Enduring Freedom (OEF/OIF) who show varying degrees of PTSD. We found BBR reflected both response direction and conflict monitoring during processing of stimuli that evoked response conflict. Impaired behavioral performance and increased peri-response BBR were related to greater posttraumatic stress symptomatology (PTSS). Critically, increased BBR mediated the link between PTSS and decreased conflict monitoring accuracy. Results suggest that poor cognitive control in PTSS reflects a failure to adaptively disinhibit target motor representations, rather than a failure to inhibit distractor representations. Thus, BBR reveal limited representation of target stimuli as a primary contributor to impaired cognitive control in PTSD. Because BBR were robustly associated with behavioral performance and exhibited high statistical reliability the index may carry utility for appraising individual differences in cognitive control in other brain disorders.

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Frontal midline theta differentiates separate cognitive control strategies while still generalizing the need for cognitive control

Cited by 39 publications

References 59 publications

Anterior Cingulate Cortex Signals the Need to Control Intrusive Thoughts during Motivated Forgetting

Anterior Cingulate Cortex Signals the Need to Control Intrusive Thoughts during Motivated Forgetting

Evoked Acute Stress Alters Frontal Midline Neural Oscillations Affecting Behavioral Inhibition in College Students

Somatomotor Beta Bursts Mediate the Negative Impact of PTSD Severity on Conflict Monitoring

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