4.7 Article

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

Journal

JOURNAL OF NEUROSCIENCE
Volume 42, Issue 21, Pages 4342-4359

Publisher

SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.1711-21.2022

Keywords

anterior cingulate cortex; dorsolateral prefrontal cortex; inhibitory control; intrusive thoughts; memory suppression; motivated forgetting

Categories

Funding

  1. National Natural Science Foundation of China [31971028]
  2. Major Project of Medicine Science and Technology of PLA [AWS17J012]
  3. UK Medical Research Council [MC-A060-5PR00]
  4. Royal Society Newton International Fellowship [NF171519]

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This study investigates how people limit awareness of unwanted memories and finds that dACC plays an important role in detecting the need for memory control, while rDLPFC counters intruding thoughts that penetrate awareness.
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 dear 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.

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