Abstract
Intrusive re-experiencing of traumatic events is a hallmark symptom of posttraumatic stress disorder, characterized by rich and vivid sensory details as reported in “flashbacks”. While prevailing models of trauma intrusions focus on dysregulated emotional processes, we hypothesize that a deficiency in intrinsic sensory inhibition could drive overactivation of sensory representations of trauma memories, precipitating sensory-rich intrusions. In a sample of combat veterans, we examined resting-state alpha (8–12 Hz) oscillatory activity (in both power and posterior→frontal connectivity), given its role in sensory cortical inhibition, in association with intrusive re-experiencing symptoms. Veterans further participated in an odor task (including both combat and non-combat odors) to assess olfactory trauma memory and emotional response. We observed an association between intrusive re-experiencing symptoms and attenuated resting-state posterior→frontal alpha connectivity, which were both correlated with olfactory trauma memory. Importantly, olfactory trauma memory was identified as a mediator of the relationship between alpha connectivity and intrusive re-experiencing, suggesting that deficits in intrinsic sensory inhibition contributed to intrusive re-experiencing of trauma via heightened trauma memory. Therefore, by permitting unfiltered sensory cues to enter information processing and activate sensory representations of trauma, sensory disinhibition can constitute a sensory mechanism of intrusive re-experiencing in trauma-exposed individuals.
Highlights
Intrusive re-experiencing of traumatic events is a hallmark symptom of posttraumatic stress disorder, characterized by rich and vivid sensory details as reported in “flashbacks”
Multiple regression analyses revealed a negative association between alpha Granger causality (GC) and intrusive re-experiencing in the left hemisphere, albeit not in the right hemisphere, after controlling for depression symptoms (Fig. 2)
Sensitivity analyses confirmed the specificity of this association to intrusive symptoms, as other posttraumatic stress disorder (PTSD) symptom clusters were not associated with alpha connectivity (p’s > 0.424)
Summary
Intrusive re-experiencing of traumatic events is a hallmark symptom of posttraumatic stress disorder, characterized by rich and vivid sensory details as reported in “flashbacks”. Complementing this deficiency in top-down prefrontal voluntary inhibition and exaggerated bottom-up limbic threat detection, the role of sensory cortical inhibition of incoming sensory cues in intrusive re-experiencing of trauma has not been fully examined This sensory mechanism draws support from the dual representation theory of PTSD, highlighting a sensory-bound representation system of threat memory (“S-memory”) that can be activated by basic sensory inputs and trigger the re-experiencing of traumatic events[11,12]. Via long-range, posterior→frontal projections, alpha oscillations mediate inhibitory bottom-up information flow from the sensory cortex to frontal regions to influence global neural activity[30,31,32,33] This long-range alpha connectivity plays a critical role in gating the entry of sensory input into downstream processing and, eventually, conscious awareness, thereby regulating perception, imagery, and working memory[34,35,36,37,38]. We hypothesize that deficient alpha activity could compromise sensory inhibition such that unfiltered sensory input would flood information processing, activating stored memory representations and eliciting vivid imagery and perception, akin to intrusive re-experiencing of trauma
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