Differential mechanisms of posterior cingulate cortex downregulation and symptom decreases in posttraumatic stress disorder and healthy individuals using real-time fMRI neurofeedback

Andrew A Nicholson, Daniela Rabellino, Maria Densmore, Paul A Frewen, David Steryl, Frank Scharnowski, Jean Théberge, Richard W J Neufeld, Christian Schmahl, Rakesh Jetly, Ruth A Lanius, Andrew A Nicholson, Daniela Rabellino, Maria Densmore, Paul A Frewen, David Steryl, Frank Scharnowski, Jean Théberge, Richard W J Neufeld, Christian Schmahl, Rakesh Jetly, Ruth A Lanius

Abstract

Background: Intrinsic connectivity networks, including the default mode network (DMN), are frequently disrupted in individuals with posttraumatic stress disorder (PTSD). The posterior cingulate cortex (PCC) is the main hub of the posterior DMN, where the therapeutic regulation of this region with real-time fMRI neurofeedback (NFB) has yet to be explored.

Methods: We investigated PCC downregulation while processing trauma/stressful words over 3 NFB training runs and a transfer run without NFB (total n = 29, PTSD n = 14, healthy controls n = 15). We also examined the predictive accuracy of machine learning models in classifying PTSD versus healthy controls during NFB training.

Results: Both the PTSD and healthy control groups demonstrated reduced reliving symptoms in response to trauma/stressful stimuli, where the PTSD group additionally showed reduced symptoms of distress. We found that both groups were able to downregulate the PCC with similar success over NFB training and in the transfer run, although downregulation was associated with unique within-group decreases in activation within the bilateral dmPFC, bilateral postcentral gyrus, right amygdala/hippocampus, cingulate cortex, and bilateral temporal pole/gyri. By contrast, downregulation was associated with increased activation in the right dlPFC among healthy controls as compared to PTSD. During PCC downregulation, right dlPFC activation was negatively correlated to PTSD symptom severity scores and difficulties in emotion regulation. Finally, machine learning algorithms were able to classify PTSD versus healthy participants based on brain activation during NFB training with 80% accuracy.

Conclusions: This is the first study to investigate PCC downregulation with real-time fMRI NFB in both PTSD and healthy controls. Our results reveal acute decreases in symptoms over training and provide converging evidence for EEG-NFB targeting brain networks linked to the PCC.

Keywords: machine learning; neurofeedback; post-traumatic stress disorder; real-time fMRI.

© 2021 The Authors. Brain and Behavior published by Wiley Periodicals LLC.

Figures

FIGURE 1
FIGURE 1
Schematic of the real‐time fMRI neurofeedback set‐up. Brain activity in the neurofeedback target region (posterior cingulate cortex) was processed in real‐time and presented to participants in the fMRI scanner as thermometers that increased or decreased as activation fluctuated. Participants completed three neurofeedback training runs and a transfer run without neurofeedback signal. Figure created with BioRender.com.
FIGURE 2
FIGURE 2
Neurofeedback experimental procedure for the regulate condition. The same timing was utilized for (i) view conditions in which participants viewed trauma‐related/distressing words while not attempting to regulate and (ii) for neutral conditions in which participants viewed neutral words and did not attempt to regulate. A trial started with a 2 s instruction slide indicating trial type (i.e., regulate, view, neutral). In the following block, participants saw either a trauma‐related/distressing word or a neutral word with a thermometer at both sides. The thermometer displayed the change in brain activation and was updated every 2 s.
FIGURE 3
FIGURE 3
(a) Event‐related BOLD response in the NFB target area (PCC), during the three training runs in the PTSD and healthy control groups. The red lines indicate PCC activation during the regulate condition, where the goal was to decrease activation while viewing trauma/stressful words. The green lines indicate PCC activation during the view condition, where participants were not attempting to decrease activation while viewing trauma/stressful words. Here, PCC activation was significantly lower during regulate as compared to view conditions for NFB training runs 1–3, for both the PTSD and healthy control groups. (b) Event‐related BOLD response in the target area (PCC) during the transfer run when neurofeedback was not provided. Taken together, this demonstrates that both groups were able to gain control over downregulating their PCC with similar success. The x‐axis of the graphs indicate time over the 24 s conditions; the y‐axis indicates the event‐related BOLD response (peristimulus time histogram) in the target area. Shaded areas of red and green indicate standard error of the mean. Abbreviations: PCC = posterior cingulate cortex, NFB = neurofeedback.
FIGURE 4
FIGURE 4
Neural dynamics during NFB training of PCC downregulation. Illustration of brain areas that show concomitant decreases in activity during regulate as compared to view conditions across NFB training runs in the PTSD group. Results evaluated at the FDR‐cluster corrected level for multiple comparisons (p < .05, k = 10). Abbreviations: PCC = posterior cingulate cortex, dmPFC = dorsomedial prefrontal cortex.
FIGURE 5
FIGURE 5
(a) Neural dynamics during NFB training of PCC downregulation. Brain areas that show concomitant decreases (blue) and increases (red) in activity during regulate as compared to view conditions across NFB training runs in the healthy control group. (b) Direct group comparisons revealed that the healthy control group displayed increased right dlPFC activation relative to the PTSD group, during regulate as compared to view conditions over NFB training. (c) Illustration of brain areas that show concomitant decreases (blue) in activity during regulate as compared to view conditions during the transfer run without neurofeedback in the healthy control group. Results evaluated at the FDR‐cluster corrected level for multiple comparisons (p < .05, k = 10). Abbreviations: NFB = neurofeedback, PCC = posterior cingulate cortex, dlPFC = dorsolateral prefrontal cortex.
FIGURE 6
FIGURE 6
The upper portion of the figure shows correlations between PTSD severity scores (CAPS total) and brain activation during NFB training. The lower portion of the figure illustrates correlations between difficulties in emotion regulation (DERS total) and brain activation during NFB training. Red clusters indicate positive correlations during view as compared to regulate conditions. Blue clusters indicate negative correlations during regulate as compared to view conditions. During NFB training, the more severe the PTSD symptoms, the more the left anterior insula and the right cerebellum (lobule VI/Crus I) was activated during view as compared to regulate conditions. Additionally, the more the dlPFC was activated during regulate as compared to view conditions over NFB training, the less severe the PTSD symptoms. Furthermore, the more difficult it was for participants to regulate their emotions, the more the anterior insula was activated during view as compared to regulate conditions. Finally, the more dlPFC activation during regulate as compared to view conditions over NFB training, the less difficulties participants had with emotion regulation. Results evaluated at the FDR‐cluster corrected level for multiple comparisons (p < .05, k = 10). NFB = neurofeedback, dlPFC = dorsolateral prefrontal cortex.
FIGURE 7
FIGURE 7
When examining state changes in emotional experience over NFB training in response to trauma/stressful stimuli presentation, we found that the PTSD and healthy control groups demonstrated significant reductions on reliving symptoms, where additionally, the PTSD group demonstrated significant reductions on distress symptoms as measured by the RSDI Scale. Abbreviations: NFB = neurofeedback, RSDI = Response to Script Driven Imagery Scale.

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