Dynamic targeting enables domain-general inhibitory control over action and thought by the prefrontal cortex

Apšvalka, Dace; Ferreira, Catarina S.; Schmitz, Taylor W.; Rowe, James B.; Anderson, Michael C.

doi:10.1038/s41467-021-27926-w

Cited by 49 publications

(51 citation statements)

References 128 publications

(201 reference statements)

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“…To confirm that suppressing associate words engaged dACC and rDLPFC, we analyzed fMRI data comparing the activation between NT and T trials from the TNT phase. Using a priori dACC and rDLPFC ROIs taken from a meta-analysis of 16 retrieval suppression studies ( Apšvalka et al, 2022 ), we observed greater activity during retrieval suppression than during voluntary retrieval (dACC: +6, +23, +41; p (FWE) < 0.05, small volume corrected (SVC); rDLPFC: +36, +38, +32; p (FWE) < 0.01, SVC). With the opposite contrast (NT < T), we also confirmed decreased activity during retrieval suppression relative to voluntary retrieval in the hippocampus (left hippocampus: −33, −34, −10; p (FWE) < 0.001, SVC; right hippocampus: +24, −25, −13; p (FWE) < 0.05, SVC).…”

Section: Resultsmentioning

confidence: 98%

“…To test our a priori hypotheses, some analyses were restricted to the dACC, rDLPFC, and bilateral hippocampus. dACC and rDLPFC masks only included subregions that are commonly activated during action cancellation and memory inhibition, revealed by meta-analyses using fMRI data from stop-signal and TNT tasks ( Guo et al, 2018 ; Apšvalka et al, 2022 ). Each mask comprised the cluster of voxels revealed by conjunction analyses combining the contrasts No-Think > Think and Stop > Go ( Guo et al, 2018 , their Fig.…”

Section: Methodsmentioning

confidence: 99%

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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: 98%

Section: Methodsmentioning

confidence: 99%

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

et al. 2022

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“…Many studies have found that memory suppression decreases hippocampal activation (see Anderson and Hulbert, 2021 for a review). Effective connectivity analyses further reveal that reduced activation of these regions is caused in part by top-down control by MFG (Benoit and Anderson, 2012; Benoit et al, 2015; Benoit et al, 2016; Gagnepain et al, 2017; Apšvalka et al, 2022). But most research focuses on a few selected ROIs, such as the right MFG as the source of modulation (Paz-Alonso et al, 2013; Yang et al, 2021) and the hippocampus as the target of down-regulation.…”

Section: Discussionmentioning

confidence: 99%

“…This phenomenon bears a striking resemblance to organic amnesias caused by damage to the hippocampus (for reviews, see Spiers et al, 2001). In fact, the amnesic shadow was predicted based on numerous reports of hippocampal deactivations (relative to the Think condition, as well as to passive baseline conditions) observed during studies of memory suppression (Anderson et al, 2004; Depue et al, 2007; Benoit and Anderson, 2012; Paz-Alonso et al, 2013; Gagnepain et al, 2014; Benoit et al, 2016; Yang et al, 2020; Apšvalka et al, 2022). Consistent with a role of hippocampal deactivations in successful memory control, hippocampal modulation is greatest (and predictive of suppression-induced forgetting) when unwanted memories intrude and need to be purged from awareness (Levy and Anderson, 2012; Gagnepain et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Reduced Hippocampal-Cortical Connectivity During Memory Suppression Predicts the Ability to Forget Unwanted Memories

Yan

Hulbert

Zhuang

et al. 2022

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The ability to suppress unwelcome memories is important for productivity and well-being. Successful memory suppression is associated with hippocampal deactivations and a concomitant disruption of this region's functionality. Much of the previous neuroimaging literature exploring such suppression-related hippocampal modulations has focused on the region's negative coupling with the prefrontal cortex. In contrast, task-based changes in functional connectivity between the hippocampus and other brain regions have remained relatively underexplored. Here, we utilize psychophysiological interactions and seed connectome-based predictive modeling (seed-CPM) to investigate the relationship between the hippocampus and the rest of the brain as 134 participants attempted to suppress unwanted memories during the Think/No-Think task. The results show that during retrieval suppression, the right hippocampus exhibited decreased functional connectivity with visual cortical areas (bilateral intracalcarine cortex, right cuneal cortex, left lingual gyrus, right supracalcarine cortex, right occipital pole), left nucleus accumbens and the brain-stem that predicted superior forgetting of unwanted memories on later memory tests. Validation tests verified that prediction performance was not an artifact of head motion or prediction method and that the negative features remained consistent across different brain parcellations. These findings suggest that systemic memory suppression involves more than the modulation of hippocampal activity—it alters functional connectivity patterns between the hippocampus and visual cortex, leading to successful forgetting.

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“…Because the inhibitory control mechanism involved in retrieval suppression is considered domain general (Anderson & Floresco, 2021; Anderson & Hulbert, 2021; Apšvalka et al, 2022; Depue et al, 2016; Gagnepain et al, 2014, 2017; Hu et al, 2017), EEG correlates of autobiographical memory control may be similar to those involved in suppressing simpler memories. Therefore, EEG correlates of autobiographical memory control may be reflected in early ERP negativities (Bergström et al, 2009b; Crespo-García et al, 2021; Mecklinger et al, 2009; Streb et al, 2016) and later sustained alpha/beta power reductions as in prior research (Legrand et al, 2020; Lin et al, 2021; Quaedflieg et al, 2020; Waldhauser et al, 2015).…”

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confidence: 99%

EEG evidence that morally relevant autobiographical memories can be suppressed

Satish

Hellerstedt

Anderson

et al. 2022

Preprint

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Remembering unpleasant events can trigger negative feelings. Fortunately, research indicates that unwanted memories can be suppressed to prevent them from intruding into awareness, improving our mental state. The current scientific understanding of memory suppression is, however, based mostly on simpler memories such as associations between words or pictures, which may not reflect how people control unpleasant memory intrusions in everyday life. Here, we investigated the neural and behavioural dynamics of suppressing personal and emotional autobiographical memories using a modified version of the Think/No-Think task. We asked participants to suppress memories of their own past immoral actions, which were hypothesised to be both highly intrusive and motivating to suppress. We report novel evidence from behavioural, ERP and EEG oscillation measures that autobiographical memory retrieval can be suppressed and suggest that autobiographical suppression recruits similar neurocognitive mechanisms as suppression of simple laboratory associations. Suppression did fail sometimes, and EEG oscillations indicated that such memory intrusions occurred from lapses in sustained control. Importantly however, participants improved at limiting intrusions with repeated practice. Furthermore, both behavioural and EEG evidence indicated that intentional suppression may be more difficult for memories of our morally wrong actions than memories of our morally right actions. The findings elucidate the neurocognitive correlates of autobiographical retrieval suppression and have implications for theories of morally motivated memory control.

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Dynamic targeting enables domain-general inhibitory control over action and thought by the prefrontal cortex

Cited by 49 publications

References 128 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

Reduced Hippocampal-Cortical Connectivity During Memory Suppression Predicts the Ability to Forget Unwanted Memories

EEG evidence that morally relevant autobiographical memories can be suppressed

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