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Altered predictive control during memory suppression in PTSD.

ABSTRACT: Aberrant predictions of future threat lead to maladaptive avoidance in individuals with post-traumatic stress disorder (PTSD). How this disruption in prediction influences the control of memory states orchestrated by the dorsolateral prefrontal cortex is unknown. We combined computational modeling and brain connectivity analyses to reveal how individuals exposed and nonexposed to the 2015 Paris terrorist attacks formed and controlled beliefs about future intrusive re-experiencing implemented in the laboratory during a memory suppression task. Exposed individuals with PTSD used beliefs excessively to control hippocampal activity during the task. When this predictive control failed, the prediction-error associated with unwanted intrusions was poorly downregulated by reactive mechanisms. This imbalance was linked to higher severity of avoidance symptoms, but not to general disturbances such as anxiety or negative affect. Conversely, trauma-exposed participants without PTSD and nonexposed individuals were able to optimally balance predictive and reactive control during the memory suppression task. These findings highlight a potential pathological mechanism occurring in individuals with PTSD rooted in the relationship between the brain's predictive and control mechanisms.

SUBMITTER: Leone G

PROVIDER: S-EPMC9177681 | biostudies-literature | 2022 Jun

REPOSITORIES: biostudies-literature

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Altered predictive control during memory suppression in PTSD.

Leone Giovanni G Postel Charlotte C Mary Alison A Fraisse Florence F Vallée Thomas T Viader Fausto F de La Sayette Vincent V Peschanski Denis D Dayan Jaques J Eustache Francis F Gagnepain Pierre P

Nature communications 20220608 1

Aberrant predictions of future threat lead to maladaptive avoidance in individuals with post-traumatic stress disorder (PTSD). How this disruption in prediction influences the control of memory states orchestrated by the dorsolateral prefrontal cortex is unknown. We combined computational modeling and brain connectivity analyses to reveal how individuals exposed and nonexposed to the 2015 Paris terrorist attacks formed and controlled beliefs about future intrusive re-experiencing implemented in ...[more]

PMID: 35676268

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Project description:Auditory working memory (WM) processing in everyday acoustic environments depends on our ability to maintain relevant information online in our minds, and to suppress interference caused by competing incoming stimuli. A challenge in communication settings is that the relevant content and irrelevant inputs may emanate from a common source, such as a talkative conversationalist. An open question is how the WM system deals with such interference. Will the distracters become inadvertently filtered before processing for meaning because the primary WM operations deplete all available processing resources? Or are they suppressed post perceptually, through an active control process? We tested these alternative hypotheses by measuring magnetoencephalography (MEG), EEG, and functional MRI (fMRI) during a phonetic auditory continuous performance task. Contextual WM maintenance load was manipulated by adjusting the number of "filler" letter sounds in-between cue and target letter sounds. Trial-to-trial variability of pre- and post-stimulus activations in fMRI-informed cortical MEG/EEG estimates was analyzed within and across 14 subjects using generalized linear mixed effect (GLME) models. High contextual WM maintenance load suppressed left auditory cortex (AC) activations around 250-300 ms after the onset of irrelevant phonetic sounds. This effect coincided with increased 10-14 Hz alpha-range oscillatory functional connectivity between the left dorsolateral prefrontal cortex (DLPFC) and left AC. Suppression of AC responses to irrelevant sounds during active maintenance of the task context also correlated with increased pre-stimulus 7-15 Hz alpha power. Our results suggest that under high auditory WM load, irrelevant sounds are suppressed through a "late" active suppression mechanism, which prevents short-term consolidation of irrelevant information without affecting the initial screening of potentially meaningful stimuli. The results also suggest that AC alpha oscillations play an inhibitory role during auditory WM processing.

Project description:BackgroundPosttraumatic stress disorder (PTSD) has been found to be associated with emotion under-modulation from the prefrontal cortex and a breakdown of the top-down control of cognition and emotion. Novel adjunct therapies such as neurofeedback (NFB) have been shown to normalize aberrant neural circuits that underlie PTSD psychopathology at rest. However, little evidence exists for NFB-linked neural improvements under emotionally relevant cognitive load. The current study sought to address this gap by examining the effects of alpha-down NFB in the context of an emotional n-back task.MethodsWe conducted a 20-week double-blind randomized, sham-controlled trial of alpha-down NFB and collected neuroimaging data before and after the NFB protocol. Participants performed an emotional 1-back and 2-back working memory task, with interleaved trauma-neutral and trauma-relevant cues in the fMRI scanner. Data from 35 participants with a primary diagnosis of PTSD were analyzed in this study (n = 18 in the experimental group undergoing alpha-down NFB, n = 17 in the sham-control group).ResultsFirstly, within-group analyses showed clinically significant reductions in PTSD symptom severity scores at the post-intervention timepoint and 3-month follow-up for the experimental group, and not for the sham-control group. The neuroimaging analyses revealed that alpha-down NFB enhanced engagement of top-down cognitive and emotional control centers, such as the dorsolateral prefrontal cortex (dlPFC), and improved integration of the anterior and posterior parts of the default mode network (DMN). Finally, our results also indicate that increased alpha-down NFB performance correlated with increased activity in brain regions involved in top-down control and bodily consciousness/embodied processing of self (TPJ and posterior insula).ConclusionThis is the first study to provide mechanistic insights into how NFB may normalize dysfunctional brain activity and connectivity in PTSD under cognitive load with simultaneous symptom provocation, adding to a growing body of evidence supporting the therapeutic neuromodulatory effects of NFB. This preliminary study highlights the benefits of alpha-down NFB training as an adjunctive therapy for PTSD and warrants further investigation into its therapeutic effects on cognitive and emotion control in those with PTSD.

Dataset Information

Altered predictive control during memory suppression in PTSD.

Publications

Altered predictive control during memory suppression in PTSD.

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