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

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cam.depositDate2022-06-20
cam.issuedOnline2022-04-18
dc.contributor.authorCrespo-García, Maité
dc.contributor.authorWang, Yulin
dc.contributor.authorJiang, Mojun
dc.contributor.authorAnderson, Michael C
dc.contributor.authorLei, Xu
dc.contributor.orcidAnderson, Mike [0000-0001-9505-9299]
dc.date.accessioned2022-06-21T23:30:34Z
dc.date.available2022-06-21T23:30:34Z
dc.date.issued2022-05-25
dc.date.updated2022-06-20T14:06:21Z
dc.description.abstractHow 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.
dc.format.mediumPrint-Electronic
dc.identifier.doi10.17863/CAM.85678
dc.identifier.eissn1529-2401
dc.identifier.issn0270-6474
dc.identifier.urihttps://www.repository.cam.ac.uk/handle/1810/338270
dc.language.isoeng
dc.publisherSociety for Neuroscience
dc.publisher.departmentMrc Cognition And Brain Sciences Unit
dc.publisher.urlhttp://dx.doi.org/10.1523/jneurosci.1711-21.2022
dc.rightsAttribution 4.0 International
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/
dc.subjectanterior cingulate cortex
dc.subjectdorsolateral prefrontal cortex
dc.subjectinhibitory control
dc.subjectintrusive thoughts
dc.subjectmemory suppression
dc.subjectmotivated forgetting
dc.subjectFemale
dc.subjectGyrus Cinguli
dc.subjectHippocampus
dc.subjectHumans
dc.subjectInhibition, Psychological
dc.subjectMagnetic Resonance Imaging
dc.subjectMale
dc.subjectMental Recall
dc.subjectPrefrontal Cortex
dc.titleAnterior Cingulate Cortex Signals the Need to Control Intrusive Thoughts during Motivated Forgetting.
dc.typeArticle
dcterms.dateAccepted2022-02-22
prism.endingPage4359
prism.issueIdentifier21
prism.publicationDate2022
prism.publicationNameJ Neurosci
prism.startingPage4342
prism.volume42
pubs.funder-project-idMedical Research Council (MC_UU_00005/1)
pubs.licence-display-nameApollo Repository Deposit Licence Agreement
pubs.licence-identifierapollo-deposit-licence-2-1
rioxxterms.typeJournal Article/Review
rioxxterms.versionVoR
rioxxterms.versionofrecord10.1523/JNEUROSCI.1711-21.2022

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