The Neural Circuitry of Sensory Processing in Post-traumatic Stress Disorder
Abstract
Background: Traumatic experiences can have severe emotional and psychological consequences, which may affect the capacity to process both internal and external sensory information. Such aberrations may have cascading effects in individuals with post-traumatic stress disorder (PTSD), where alterations in sensory processing may hinder the capacity for higher-order executive functions, including emotion regulation. Delineating the neural circuitry of subcortical and cortical structures thought to be central to sensory processing is therefore critical to the study of PTSD and may help to develop an understanding of the neurobiological mechanisms underlying this often debilitating disorder.
Methods: Various neuroimaging approaches were employed to investigate sensory processing in PTSD, its dissociative subtype, and healthy controls. First, resting-state connectivity patterns of subcortical brainstem structures linked to interoceptive and exteroceptive sensory processing, including the periaqueductal gray and the vestibular nuclei, were examined (chapters 2 and 3). In addition, given that the insula is critical for relaying exteroceptive and interoceptive sensory information to other neurocognitive networks in the brain, resting-state whole brain seed-based connectivity patterns of different insula subregions were investigated (chapter 4). Furthermore, machine learning analyses were used to assess the utility of insula subregion resting-state connectivity patterns as a diagnostic predictor for classifying PTSD, its dissociative subtype, and healthy controls. Finally, a task-based paradigm using oculomotor stimuli with simultaneous traumatic autobiographical memory recall was employed to examine cortical brain structures involved in the convergence of exteroceptive and interoceptive sensory information (chapter 5).
Results and Discussion: As compared to controls, widespread periaqueductal gray connectivity was observed with cortical structures associated with emotional reactivity and defensive responding in PTSD and its dissociative subtype at rest. In addition, as compared to controls, decreased vestibular nuclei connectivity with cortical structures essential to exteroceptive sensory processing and multisensory integration was observed in individuals with the PTSD dissociative subtype. Moreover, PTSD showed limited cortical insula subregion resting-state connectivity with frontal lobe structures involved in the central executive network, which may be associated with impairment of higher-order executive functions, including emotion regulation, in PTSD. Finally, exposure to simultaneous exteroceptive and interoceptive sensory stimuli through oculomotor eye movements performed simultaneous to traumatic memory recall engaged the dorsal attentional network and default-mode frontoparietal networks that have been demonstrated to work in tandem to facilitate connectivity with structures in the central executive network, including the dorsolateral and dorsomedial prefrontal cortex, necessary for multisensory integration and emotion regulation. This effect was greater in individuals with PTSD and may provide a neurobiological account for how oculomotion may influence the frontoparietal cortical representation of traumatic memories. Overall, the findings of this dissertation reveal that individuals with PTSD experience aberrations in the neural circuitry necessary for processing both interoceptive and exteroceptive sensory information. We hypothesize that these observed alterations in interoceptive and exteroceptive neural processing may underlie, in part, the emotion dysregulation and maladaptive responses to chronic stress, including hypervigilance and dissociative symptoms, observed in PTSD and its dissociative subtype.