Male veterans with PTSD exhibit aberrant neural dynamics during working memory processing: an MEG study

Abstract

IntroductionPosttraumatic stress disorder (PTSD) is a psychiatric disorder characterized by re-experiencing, avoidance, negative alterations in mood and cognition, and physiologic arousal symptoms, which may develop subsequent to a traumatic event (e.g., combat).1,2 The lifetime prevalence of PTSD in the United States is roughly 7%-9%; 3,4 however, prevalence rates among recent combat veterans are estimated at 13%-22%. 5,6 Previous studies have demonstrated that patients with PTSD experience deficits in memory, attention and executive functioning. [7][8][9] More specifically, a recent meta-analysis of 60 neurocognitive studies comparing patients with PTSD to healthy controls (4108 participants) found the largest effect sizes reflecting deficiencies in the PTSD group for verbal learning, information processing speed and attention/working memory. 10 The etiology of these functional deficits is not entirely clear, but they do appear to be contributing factors to PTSD symptomatology. 11,12Working memory is an essential component of information processing and is typically divided into 3 cognitive subprocesses: encoding, maintenance and retrieval.13 Studies using functional magnetic resonance imaging (fMRI) and positron emission tomography 14 have identified the network architecture serving working memory processing in healthy adults. Critical brain regions include the prefrontal cortex, superior parietal lobule and adjacent areas, lateral occipital regions, cerebellum, and the left supramarginal gyrus and contiguous temporal regions.14,15 While such studies elucidate brain regions responsible for general working memory function, they rely on indirect measures of brain activity (e.g., local blood oxygenation), making it difficult to dissociate which areas are active during each phase of working memory. Background: Posttraumatic stress disorder (PTSD) is associated with executive functioning deficits, including disruptions in working memory. In this study, we examined the neural dynamics of working memory processing in veterans with PTSD and a matched healthy control sample using magnetoencephalography (MEG). Methods: Our sample of recent combat veterans with PTSD and demographically matched participants without PTSD completed a working memory task during a 306-sensor MEG recording. The MEG data were preprocessed and transformed into the time-frequency domain. Significant oscillatory brain responses were imaged using a beamforming approach to identify spatiotemporal dynamics. Results: Fifty-one men were included in our analyses: 27 combat veterans with PTSD and 24 controls. Across all participants, a dynamic wave of neural activity spread from posterior visual cortices to left frontotemporal regions during encoding, consistent with a verbal working memory task, and was sustained throughout maintenance. Differences related to PTSD emerged during early encoding, with patients exhibiting stronger α oscillatory responses than controls in the right inferior frontal gyrus (IFG). Differences spread to the right supramarginal ...

Neuroimaging with magnetoencephalography: A dynamic view of brain pathophysiology

“…66 A new study of verbal working memory from our laboratory reached a similar conclusion, as veterans with PTSD exhibited normal responses during both encoding and maintenance operations in left hemispheric language regions, but disturbed responses in right inferior frontal, right supramarginal and superior temporal cortices throughout the majority of encoding and maintenance periods (see Figure 5). 67 As with other studies, these right hemispheric responses correlated with PTSD symptom severity, and we propose that such activity in homologue areas reflects compensatory processing in veterans with PTSD. 67 In a follow-up study, we showed that attention training treatment sharply reduced PTSD symptom severity and largely normalized neural activity in these same brain regions during verbal working memory processing.…”

“…67 As with other studies, these right hemispheric responses correlated with PTSD symptom severity, and we propose that such activity in homologue areas reflects compensatory processing in veterans with PTSD. 67 In a follow-up study, we showed that attention training treatment sharply reduced PTSD symptom severity and largely normalized neural activity in these same brain regions during verbal working memory processing. 68 …”

“…Note that right hemispheric group differences were observed in other time periods (not shown) as well. 67 …”

Attention training improves aberrant neural dynamics during working memory processing in veterans with PTSD

“…This study found aberrant oscillatory alpha activity during WM encoding and maintenance in veterans with PTSD. These significant differences in oscillatory activity were found in the right inferior frontal gyrus (IFG), right supramarginal gyrus (SMG), and right inferior parietal areas (McDermott et al, 2015). In this study, we examined whether these neural abnormalities in WM processing could be ameliorated with attention training treatment by collecting pre- and posttreatment MEG recordings from a group of veterans who participated in a recent clinical trial of attention training for PTSD (Badura-Brack et al, 2015).…”

“…Briefly, we compared pre- and posttreatment recordings from the veterans with PTSD to a control sample of psychologically healthy combat-exposed veterans who completed the identical WM task during a single MEG session. The pretreatment recordings of the veterans with PTSD and the data from the healthy combat-exposed veterans were both a subset of the data reported in McDermott and colleagues (2015), although that study did not examine treatment effects and included additional controls that had not been exposed to combat or any type of trauma. The current study accounted for combat exposure by using a control group comprised only of combat veterans without PTSD.…”