Resting‐state pulvinar‐posterior parietal decoupling in PTSD and its dissociative subtype

Terpou, Braeden A.; Densmore, Maria; Théberge, Jean; Frewen, Paul A.; McKinnon, Margaret C.; Lanius, Ruth A.

doi:10.1002/hbm.24242

Cited by 30 publications

(31 citation statements)

References 102 publications

(197 reference statements)

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“…Although the Brainnetome atlas was used to parcellate the insula into its subregions (not captured in the Automated Anatomical Labeling [AAL] atlas and MNI2 Talairich [MNI2Tal] atlas), brain regions from the results of the seed‐based analysis were identified using the AAL atlas (Tzourio‐Mazoyer et al, ) via xjview software (https://www.nitrc.org/projects/xjview), the MNI2Tal atlas (https://bioimagesuite.yale.edu/mni2tal; Lacadie, Fulbright, Constable, & Papademetris, ), and visual inspection using an additional anatomical atlas (Montemurro & Bruni, ). This approach is consistent with our previous studies (Harricharan et al, ; Rabellino et al ; Terpou et al, ).…”

Section: Methodssupporting

confidence: 94%

“…Seedbased analysis correlations with self-reported psychological measures used to assess state symptoms at the time of scanning (RSDI, STAI, CADSS) and trait symptoms prior to scanning (CAPS, CTQ, MDI, BDI) were performed in both the PTSD and PTSD+DS groups (significant peak coordinates were evaluated at the same voxel-wise pFWE < .05, k = 10 threshold and visual inspection using an additional anatomical atlas (Montemurro & Bruni, 1988). This approach is consistent with our previous studies (Harricharan et al, 2016;Rabellino et al 2018;Terpou et al, 2018).…”

Section: Full Factorial Analysissupporting

confidence: 93%

“…A primary PTSD diagnosis was determined using the Clinician‐Administered PTSD Scale (CAPS), versions IV (for 156 participants) and 5 (for 28 participants)—CAPS IV: cutoff score > 50 (Blake et al, ); CAPS‐5: no cutoff score is used for the DSM‐5 version (Weathers et al, ). Individuals meeting the criteria for the dissociative subtype scored at least 2 in frequency and intensity on the CAPS‐IV scale or at least 2 in symptom severity on the CAPS‐5 scale for depersonalization and/or derealization symptoms as per previous studies (Harricharan et al, ; Rabellino et al, ; Terpou et al, ). For all participants, the SCID (Structured Clinical Interview for DSM‐IV Axis I disorders; First, Spitzer, Gibbon, & Williams, ) was administered, along with a battery of questionnaires: Beck Depression Inventory (BDI; Beck, Guth, Steer, & Ball, ), Child Trauma Questionnaire (CTQ; 87% of all PTSD patients had histories of childhood trauma, confirmed if patient scored above the none/minimal threshold for any trauma category according to the CTQ scoring manual; Bernstein & Fink, ), as well as the Multiscale Dissociation Inventory (MDI; Briere, Weathers, & Runtz, ).…”

Section: Methodsmentioning

confidence: 99%

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PTSD and its dissociative subtype through the lens of the insula: Anterior and posterior insula resting‐state functional connectivity and its predictive validity using machine learning

et al. 2019

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Individuals with post‐traumatic stress disorder (PTSD) typically experience states of reliving and hypervigilance; however, the dissociative subtype of PTSD (PTSD+DS) presents with additional symptoms of depersonalization and derealization. Although the insula is critical to emotion processing, its association with these contrasting symptom profiles is yet to be fully delineated. Accordingly, we investigated insula subregion resting‐state functional connectivity patterns among individuals with PTSD, PTSD+DS, and healthy controls. Using SPM12 and PRONTO software, we implemented a seed‐based resting‐state functional connectivity approach, along with multiclass Gaussian process classification machine learning, respectively, in order to evaluate unique patterns and the predictive validity of insula subregion connectivity among individuals with PTSD (n = 84), PTSD+DS (n = 49), and age‐matched healthy controls (n = 51). As compared to PTSD and PTSD+DS, healthy controls showed increased right anterior and posterior insula connectivity with frontal lobe structures. By contrast, PTSD showed increased bilateral posterior insula connectivity with subcortical structures, including the periaqueductal gray. Strikingly, as compared to PTSD and controls, PTSD+DS showed increased bilateral anterior and posterior insula connectivity with posterior cortices, including the left lingual gyrus and the left precuneus. Moreover, machine learning analyses were able to classify PTSD, PTSD+DS, and controls using insula subregion connectivity patterns with 80.4% balanced accuracy (p < .01). These findings suggest a neurobiological distinction between PTSD and its dissociative subtype with regard to insula subregion functional connectivity patterns. Furthermore, machine learning algorithms were able to utilize insula resting‐state connectivity patterns to discriminate between participant groups with high predictive accuracy.

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Section: Methodssupporting

confidence: 94%

Section: Full Factorial Analysissupporting

confidence: 93%

Section: Methodsmentioning

confidence: 99%

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PTSD and its dissociative subtype through the lens of the insula: Anterior and posterior insula resting‐state functional connectivity and its predictive validity using machine learning

et al. 2019

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“…In effect, subcortical systems functioning with reduced cortical input may form defensive responses stored in subcortical “loops” within the midbrain (Lanius, Paulson, et al, ). Here, the thalamus serves as a mediator between the cortex and the lower‐level systems and the thalamus has further been demonstrated to display altered functionality in PTSD and its dissociative subtype (Lanius et al, ; Terpou et al, ). Specifically, the thalamus shows less activation in PTSD as compared to controls (Lanius et al, ), a finding supported by a previous meta‐analysis pointing toward thalamic hypoactivation in general in PTSD (Etkin & Wagner, ).…”

Section: Tonic Immobilitymentioning

confidence: 99%

The effects of trauma on brain and body: A unifying role for the midbrain periaqueductal gray

Terpou

Harricharan

McKinnon

et al. 2019

J of Neuroscience Research

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Post-traumatic stress disorder (PTSD), a diagnosis that may follow the experience of trauma, has multiple symptomatic phenotypes. Generally, individuals with PTSD display symptoms of hyperarousal and of hyperemotionality in the presence of fearful stimuli. A subset of individuals with PTSD; however, elicit dissociative symptomatology (i.e., depersonalization, derealization) in the wake of a perceived threat. This pattern of response characterizes the dissociative subtype of the disorder, which is often associated with emotional numbing and hypoarousal. Both symptomatic phenotypes exhibit attentional threat biases, where threat stimuli are processed preferentially leading to a hypervigilant state that is thought to promote defensive behaviors during threat processing. Accordingly, PTSD and its dissociative subtype are thought to differ in their proclivity to elicit active (i.e., fight, flight) versus passive (i.e., tonic immobility, emotional shutdown) defensive responses, which are characterized by the increased and the decreased expression of the sympathetic nervous system, respectively. Moreover, active and passive defenses are accompanied by primarily endocannabinoid-and opioid-mediated analgesics, respectively. Through critical review of the literature, we apply the defense cascade model to better understand the pathological presentation of defensive responses in PTSD with a focus on the functioning of lower-level midbrain and extended brainstem systems. K E Y W O R D Sbrainstem, dissociation, periaqueductal gray, PTSD, trauma | INTRODUC TI ONIn this review, we integrate literature from trauma experiences, the defense cascade, and the threat-response neurocircuitry within a framework of post-traumatic stress disorder (PTSD). We begin by introducing the concepts of the hypothalamic-pituitary-adrenal (HPA) axis, general PTSD, and defensive responses. Following these primers, we discuss the influences of trauma onset and prolonged exposure to trauma and their effects on the development of PTSD and the dissociative subtype of PTSD. Next, we introduce the defense cascade model and its underlying neurocircuitry as described in the animal literature and relate it to PTSD. In addition, we discuss the current state of the neuroimaging literature, which Edited by Sandra Chanraud.All peer review communications can be found with the online version of the article. | 1111TERPOU ET al. suggests that functional alterations are detectable in the midbrain of individuals with PTSD and its dissociative subtype as compared to healthy controls. We conclude by presenting directions for future research and the clinical implications for treatment of persons with PTSD that arise from this review of the extant literature.

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“…These studies explored the role of pulvinar under specific task conditions, leaving open the question as to whether the pulvinar influence on cortico-cortical functional connectivity is related to engagement in specific tasks, or rather a more basic property of large-scale network connectivity. Studies in humans have suggested functional connectivity between pulvinar and cortical areas even in the absence of any active task structure, based on BOLD responses (Stein, 2000;Barron, 2015;Terpou, 2018). Watching short movie clips during the data collection keeps subjects more engaged and has been shown to be a reliable method for obtaining functional connectivity data both in monkeys (Mantini, 2013) and in humans (Vanderwal, 2015;Vanderwal, 2019).…”

Section: Discussionmentioning

confidence: 99%

A causal role for pulvinar in coordinating task independent cortico-cortical interactions

Eradath

Pinsk

Kästner

2020

Preprint

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planned and conceptualized the study. M. K. E and M. A. P performed the experiments. M. K. E and M. A. P performed analysis. M. K. E. and S. K. prepared the draft. M. K. E, M. A. P and S. K. reviewed and edited the final draft. AbstractPulvinar is the largest nucleus in the primate thalamus and has topographically organized connections with multiple cortical areas, thereby forming extensive cortico-pulvino-cortical input-output loops. Neurophysiological studies have provided evidence for a role of these transthalamic pathways in regulating information transmission between cortical areas. However, a causal role of pulvinar in regulating cortico-cortical interactions has not yet been demonstrated. In particular, it is not known whether pulvinar's influences on cortical networks are taskdependent or reflect more basic large-scale network properties that maintain functional connectivity across a network regardless of active task demands. In the current study, under a passive viewing condition, we conducted simultaneous electrophysiological recordings from interconnected ventral (area V4) and dorsal (LIP) nodes of the macaque visual system while reversibly inactivating the dorsal part of lateral pulvinar (dPL), which shares common anatomical connectivity with V4 and LIP. Our goal was to probe a causal role of pulvinar in regulating cortico-cortical interactions in the absence of any active task demands. Our results show a significant reduction in local field potential phase coherence between LIP and V4 in low frequencies (4-15 Hz) following muscimol -a potent GABAA agonist -injection into dPL. At the local level, no significant changes in firing rates or LFP power were observed in LIP or in V4 following dPL inactivation. These results indicate a causal role for pulvinar in synchronizing neural activity between interconnected cortical nodes of a large-scale network, even in the absence of an active task state. Significance StatementPulvinar, the largest nucleus of the primate thalamus, has been implicated in several cognitive functions. The extensive cortico-pulvino-cortical loops formed by pulvinar are suggested to be regulating information transmission between interconnected cortical areas. However, a causal evidence for pulvinar's role in cortico-cortical interactions in the absence of active task demands is not yet clear. We conducted simultaneous recordings from nodes of macaque visual system (areas V4 and LIP) while inactivating the dorsal part of the lateral pulvinar (dPL) under a passive viewing condition. Our results show a significant reduction in local field phase coherence between LIP and V4 in low frequencies ( 4-15 Hz) following inactivation of dPL, thus providing evidence for a causal role of pulvinar in regulating cortico-cortical interactions even in the absence of an active task state.

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Resting‐state pulvinar‐posterior parietal decoupling in PTSD and its dissociative subtype

Cited by 30 publications

References 102 publications

PTSD and its dissociative subtype through the lens of the insula: Anterior and posterior insula resting‐state functional connectivity and its predictive validity using machine learning

PTSD and its dissociative subtype through the lens of the insula: Anterior and posterior insula resting‐state functional connectivity and its predictive validity using machine learning

The effects of trauma on brain and body: A unifying role for the midbrain periaqueductal gray

A causal role for pulvinar in coordinating task independent cortico-cortical interactions

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