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Restless 'rest'

Title: Restless 'rest': intrinsic sensory hyperactivity and disinhibition in post-traumatic stress disorder.
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Name(s): Clancy, Kevin, author
Ding, Mingzhou, author
Bernat, Edward, author
Schmidt, Norman B, author
Li, Wen, author
Type of Resource: text
Genre: Journal Article
Text
Date Issued: 2017-07-01
Physical Form: computer
online resource
Extent: 1 online resource
Language(s): English
Abstract/Description: Post-traumatic stress disorder is characterized by exaggerated threat response, and theoretical accounts to date have focused on impaired threat processing and dysregulated prefrontal-cortex-amygdala circuitry. Nevertheless, evidence is accruing for broad, threat-neutral sensory hyperactivity in post-traumatic stress disorder. As low-level, sensory processing impacts higher-order operations, such sensory anomalies can contribute to widespread dysfunctions, presenting an additional aetiological mechanism for post-traumatic stress disorder. To elucidate a sensory pathology of post-traumatic stress disorder, we examined intrinsic visual cortical activity (based on posterior alpha oscillations) and bottom-up sensory-driven causal connectivity (Granger causality in the alpha band) during a resting state (eyes open) and a passive, serial picture viewing state. Compared to patients with generalized anxiety disorder (n = 24) and healthy control subjects (n = 20), patients with post-traumatic stress disorder (n = 25) demonstrated intrinsic sensory hyperactivity (suppressed posterior alpha power, source-localized to the visual cortex-cuneus and precuneus) and bottom-up inhibition deficits (reduced posterior→frontal Granger causality). As sensory input increased from resting to passive picture viewing, patients with post-traumatic stress disorder failed to demonstrate alpha adaptation, highlighting a rigid, set mode of sensory hyperactivity. Interestingly, patients with post-traumatic stress disorder also showed heightened frontal processing (augmented frontal gamma power, source-localized to the superior frontal gyrus and dorsal cingulate cortex), accompanied by attenuated top-down inhibition (reduced frontal→posterior causality). Importantly, not only did suppressed alpha power and bottom-up causality correlate with heightened frontal gamma power, they also correlated with increased severity of sensory and executive dysfunctions (i.e. hypervigilance and impulse control deficits, respectively). Therefore, sensory aberrations help construct a vicious cycle in post-traumatic stress disorder that is in action even at rest, implicating dysregulated triangular sensory-prefrontal-cortex-amygdala circuitry: intrinsic sensory hyperactivity and disinhibition give rise to frontal overload and disrupt executive control, fuelling and perpetuating post-traumatic stress disorder symptoms. Absent in generalized anxiety disorder, these aberrations highlight a unique sensory pathology of post-traumatic stress disorder (ruling out effects merely reflecting anxious hyperarousal), motivating new interventions targeting sensory processing and the sensory brain in these patients.
Identifier: FSU_pmch_28582479 (IID), 10.1093/brain/awx116 (DOI), PMC6059177 (PMCID), 28582479 (RID), 28582479 (EID), 3860546 (PII)
Keywords: Granger causality, Alpha/gamma oscillations, Post-traumatic stress disorder (PTSD), Resting state, Sensory hyperactivity
Grant Number: R01 MH093413, T32 DC000044
Publication Note: This NIH-funded author manuscript originally appeared in PubMed Central at https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6059177.
Subject(s): Adult
Alpha Rhythm/physiology
Anxiety Disorders/physiopathology
Case-Control Studies
Executive Function/physiology
Female
Frontal Lobe/physiopathology
Gamma Rhythm/physiology
Gyrus Cinguli/physiopathology
Humans
Male
Neural Inhibition/physiology
Photic Stimulation
Rest/physiology
Sensation Disorders/complications
Sensation Disorders/physiopathology
Stress Disorders, Post-Traumatic/complications
Stress Disorders, Post-Traumatic/physiopathology
Visual Cortex/physiopathology
Visual Perception/physiology
Young Adult
Persistent Link to This Record: http://purl.flvc.org/fsu/fd/FSU_pmch_28582479
Owner Institution: FSU
Is Part Of: Brain : a journal of neurology.
1460-2156
Issue: iss. 7, vol. 140

Choose the citation style.
Clancy, K., Ding, M., Bernat, E., Schmidt, N. B., & Li, W. (2017). Restless 'rest': intrinsic sensory hyperactivity and disinhibition in post-traumatic stress disorder. Brain : A Journal Of Neurology. Retrieved from http://purl.flvc.org/fsu/fd/FSU_pmch_28582479