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

Abstract

How do people limit awareness of unwanted memories? Evidence suggests that when unwelcome memories intrude, a retrieval stopping process engages the right dorsolateral prefrontal cortex (rDLPFC; Michael C. Anderson et al., 2004) to inhibit hippocampal activity (Benoit & Anderson, 2012; Benoit, Hulbert, Huddleston, & Anderson, 2015; Gagnepain, Hulbert, & Anderson, 2017) and disrupt retrieval. It remains unknown how and when the need to engage prefrontal control is detected, and whether control operates proactively to prevent an unwelcome memory from being retrieved, or must respond reactively, to counteract its intrusion. We hypothesized that dorsal anterior cingulate cortex (dACC) achieves this function by detecting signals indicating that an unwanted trace is emerging in awareness, and transmitting the need for inhibitory control to right DLPFC (Alexander & Brown, 2011; Botvinick, Braver, Barch, Carter, & Cohen, 2001). During a memory suppression task, we measured trial-by-trial variations in dACC's theta power and N2 amplitude, two electroencephalographic (EEG) markers of the need for enhanced control (Cavanagh & Frank, 2014). With simultaneous EEG-fMRI recordings, we tracked dynamic interactions between the dACC, rDLPFC and hippocampus during suppression. EEG analyses revealed a clear role of dACC in detecting the need for memory control, and in upregulating prefrontal inhibition. Importantly, we identified dACC contributions before episodic retrieval could have occurred (500 ms) and afterwards, indicating distinct proactive and reactive control signalling. Stronger proactive control by the dACC led to reduced hippocampal activity and diminished overall blood-oxygen-level-dependent (BOLD) signal in dACC and rDLPFC, suggesting that pre-empting retrieval early reduced overall control demands. However, when dACC activity followed the likely onset of recollection, retrieval was cancelled reactively: effective connectivity analyses revealed robust communication from dACC to rDLPFC and from rDLPFC to hippocampus, 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.