Neural Networks of Information Processing in Posttraumatic Stress Disorder: A Functional Magnetic Resonance Imaging Study

doi:10.1016/j.biopsych.2005.03.021

Biological Psychiatry

Volume 58, Issue 2, 15 July 2005, Pages 111-118

https://doi.org/10.1016/j.biopsych.2005.03.021 Get rights and content

Background

Neuroimaging studies report reduced medial prefrontal cortical (particularly anterior cingulate) but enhanced amygdala response to fear signals in posttraumatic Stress Disorder (PTSD). We investigated whether anterior cingulate-amygdala dysregulation in PTSD would generalize to salient, but nonthreat related signals.

Methods

Individuals with PTSD (n = 14) and age and sex-matched nontraumatized controls (n = 14) completed an auditory oddball paradigm adapted to functional magnetic resonance imaging at a 1.5-T field strength.

Results

Controls displayed bilateral activation in ventral anterior cingulate and amygdala networks, and PTSD subjects showed bilateral dorsal anterior cingulate and amygdala activation to targets relative to nontargets. Compared to controls, PTSD subjects showed enhanced responses to targets in the dorsal and rostral anterior cingulate, and left amygdala. Whole-brain analyses confirmed the expected pattern of distributed prefrontal-parietal responses to targets in the oddball task. Greater activity in posterior parietal somatosensory regions was observed in PTSD.

Conclusions

Our findings of enhanced anterior cingulate responses in PTSD contrast with reports of reduced activity for threat stimuli, suggesting that the latter may be specific to processing of threat-related content. Activation in rostral and dorsal anterior cingulate, left amygdala and posterior parietal networks in response to salient, nonthreatening stimuli may reflect generalized hypervigilance.

Section snippets

Participants

Fourteen individuals with PTSD (8 male/6 female) and 14 age and sex-matched nontraumatized controls were recruited for the study. Participants with PTSD were recruited from a treatment-seeking sample at the Westmead Hospital PTSD Unit and nontraumatized controls were recruited from community samples. Nine participants with PTSD were survivors of interpersonal assault, and 5 had survived motor vehicle accidents. The average time post-trauma was 73.4 months (SD = 75.7, range 6.3–202 months). PTSD

Reaction-Time Data

Reaction time data were missing for three PTSD participants and four controls due to technical or behavioral error. A one-way analysis of variance revealed no significant differences in reaction times between groups (F (1,19) = 3.39, p = .08), although there was a trend for the PTSD group (mean 368.7 msec; SD 153.7) to have faster RT than controls (mean 486 msec; SD 136.6).

Clinical Data

PTSD participants revealed significantly greater scores on the depression (t(1,26) = 18.1, p < .001) and anxiety (t(1,26) =

Discussion

The current findings accord with previously reported responses of the dorsal (cognitive) and ventral-rostral (affective) components of the ACC (Bush et al., 2000, Devinsky et al., 1995). Whereas the dorsal ACC is activated during cognitive tasks (Bush et al 1998), the rostral ACC is particularly activated during emotional processing (Whalen et al 1998). The current findings indicate that, in contrast to previous reports of diminished rostral ACC recruitment during threat/emotional processing in

References (53)

G. Aston-Jones et al.
Role of locus coeruleus in attention and behavioral flexibility
Biol Psychiatry
(1999)
J. Attias et al.
Event-related potentials in post-traumatic stress disorder of combat origin
Biol Psychiatry
(1996)
J.D. Bremner
Does stress damage the brain?
Biol Psychiatry
(1999)
J.D. Bremner et al.
Neural correlates of exposure to traumatic pictures and sound in vietnam combat veterans with and without posttraumatic stress disorder: A positron emission tomography study
Biol Psychiatry
(1999)
J.D. Bremner et al.
Neural correlates of the classic colour and emotional stroop in women with abuse-related posttraumatic stress disorder
Biol Psychiatry
(2004)
G. Bush et al.
Cognitive and emotional influences in anterior cingulate cortex
Trends Cogn Sci
(2000)
C.R. Clark et al.
Cerebral function in posttraumatic stress disorder during verbal working memory updating: a positron emission tomography study
Biol Psychiatry
(2003)
R.J. Davidson et al.
The functional neuroanatomy of emotion and affective style
Trends Cogn Sci
(1999)
M. Kimble et al.
Stimulus novelty differentially affects attentional allocation in PTSD
Biol Psychiatry
(2000)
R.A. Lanius et al.
Brain activation during script-driven imagery induced dissociative responses in PTSD: a functional magnetic resonance imaging investigation
Biol Psychiatry
(2002)

P.F. Lovibond et al.

The structure of negative emotional states: Comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories

Behav Res Ther

(1995)

A.C. McFarlane et al.

Abnormal stimulus processing in posttraumatic stress disorder

Biol Psychiatry

(1993)

T.C. Neylan et al.

Sensory gating in chronic posttraumatic stress disorder: reduced auditory P50 suppression in combat veterans

Biol Psychiatry

(1999)

B.S. Peterson et al.

An fMRI study of Stroop word-colour interference: Evidence for cingulate sub-regions subserving multiple distributed attention systems

Biol Psychiatry

(1999)

J. Polich et al.

Cognitive and behavioural determinants of P300: an integrated review

Biol Psychology

(1995)

S.L. Rauch et al.

Exaggerated amygdala response to masked fearful vs. happy facial stimuli in posttraumatic stress disorder: a functional MRI study

Biol Psychiatry

(2000)

L.M. Shin et al.

An fMRI study of anterior cingulate function in posttraumatic stress disorder

Biol Psychiatry

(2001)

S.M. Southwick et al.

Role of norepinephrine in the pathophysiology and treatment of posttraumatic stress disorder

Biol Psychiatry

(1999)

N. Tzourio-Mazoyer et al.

Automated anatomical labelling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain

Neuroimage

(2002)

P.J. Whalen et al.

The emotional counting stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division

Biol Psychiatry

(1998)

L.M. Williams et al.

Arousal dissociates amygdala and hippocampal fear responses: Evidence from simultaneous fMRI and skin conductance recording

Neuroimage

(2001)

A. Arnsten

The biology of being frazzled

Science

(1998)

A. Bechara

Neurobiology of decision-making: risk and reward

Sem Clin Neuropsychiat

(2001)

D.D. Blake et al.

A clinician rating scale for assessing current and lifetime PTSD: The CAPS-1

Behav Ther

(1990)

G. Bush et al.

Dorsal anterior cingulate cortex: A role in reward-based decision making

Proc Nat Acad Sci

(2002)

G. Bush et al.

The counting Stroop: an interference task specialized for functional neuroimaging – validation study with functional fMRI

Hum Brain Map

(1998)

Cited by (173)

Characterizing Typhoon-related Posttraumatic Stress Disorder Based on Multimodal Fusion of Structural, Diffusion, and Functional Magnetic Resonance Imaging
2024, Neuroscience
Diagnosing posttraumatic stress disorder (PTSD) using only single-modality images is controversial. We aimed to use multimodal magnetic resonance imaging (MRI) combining structural, diffusion, and functional MRI to possibly provide a more comprehensive viewpoint on the decisive characteristics of PTSD patients. Typhoon-exposed individuals with (n = 26) and without PTSD (n = 32) and healthy volunteers (n = 30) were enrolled. Five MRI features from three modalities, including two resting-state functional MRI (rs-fMRI) features (amplitude of low-frequency fluctuation, ALFF; and regional homogeneity, ReHo), one structural MRI feature (gray matter density, GM), and two diffusion tensor imaging (DTI) features (fractional anisotropy, FA; and mean diffusivity, MD) were investigated simultaneously with a multimodal canonical correlation analysis + joint independent component analysis model to identify abnormalities in the PTSD brain. We identified statistical differences between PTSD patients and healthy controls in terms of 1 rs-fMRI (ALFF, ReHo) alterations in the superior frontal gyrus, precuneus, inferior parietal lobule (IPL), anterior cingulate cortex (ACC), and posterior cingulate cortex (PCC), 2 DTI (FA, MD) changes in the pons, genu, and splenium of the corpus callosum, and 3 Structural MRI abnormalities in the precuneus, IPL, ACC, and PCC. A novel ReHo component was found to distinguish PTSD and trauma-exposed controls, including the precuneus, IPL, middle frontal gyrus, middle occipital gyrus, and cerebellum. This study reveals that PTSD individuals exhibit intertwined functional and structural anomalies within the default mode network. Some alterations within this network may serve as a potential marker to distinguish between PTSD patients and trauma-exposed controls.
Dysconnectivity of the amygdala and dorsal anterior cingulate cortex in drug-naive post-traumatic stress disorder
2021, European Neuropsychopharmacology
Convergent studies have highlighted the amygdala-based and dorsal anterior cingulate cortex (dACC)-based circuit or network dysfunction in post-traumatic stress disorder (PTSD). However, previous studies are often complicated by various traumatic types, psychiatric comorbidities, chronic illness duration, and medication effect on brain function. Besides, little is known whether the functional integration with amygdala–dACC interaction disrupted or not in PTSD. Here, we investigated effective connectivity (EC) between the amygdala-dACC and rest of the cortex by applying psycho-physiological interaction (PPI) approach to resting-state functional magnetic resonance imaging data of 63 drug-naive PTSD patients and 74 matched trauma-exposed non-PTSD controls. Pearson correlation analysis was performed between EC values extracted from regions with between-group difference and clinical profiles in PTSD patients. We observed distinct amygdala-dACC interaction pattern between PTSD group and the control group, which is composed primarily by positive EC in the former and negative in the latter. In addition, compared with non-PTSD controls, PTSD patients showed increased EC between amygdala-dACC and the prefrontal cortex, left inferior parietal lobule, and bilateral ventral occipital cortex, and decreased EC between amygdala-dACC and the left fusiform gyrus. The EC increase between amygdala-dACC and the right middle frontal gyrus was negatively correlated with the clinician-administered PTSD scale scores in PTSD patients. Aberrent communication between amgydala-dACC and brain regions involved in central executive network and visual systems might be associated with the pathophysiology of PTSD. Further, these findings suggested that dysconnectivity of the amygdala and dACC could be adapted as a relatively early course diagnostic biomarker of PTSD.
A unifying translational framework to advance treatment research for comorbid PTSD and substance use disorders
2021, Neuroscience and Biobehavioral Reviews
We provide a unifying translational framework that can be used to synthesize extant lines of human laboratory research in four neurofunctional domains that underlie the co-occurrence of posttraumatic stress and substance use disorders (PTSD+SUD). We draw upon the Alcohol and Addiction Research Domain Criteria (AARDOC) to include executive functioning, negative emotionality, reward, and added social cognition from the National Institute of Mental Health (NIMH) Research Domain Criteria into our framework. We review research findings across each of the four domains, emphasizing human experimental studies in PTSD, SUD, and PTSD+SUD for each domain. We also discuss the implications of research findings for treatment development by considering new ways of conceptualizing risk factors and outcomes at the level of the individual patient, which will enhance treatment matching and advance innovations in intervention.
Randomized-controlled trial of response inhibition training for individuals with PTSD and impaired response inhibition
2021, Behaviour Research and Therapy
Deficits in response inhibition, defined as an inability to stop a behavior that is no longer relevant, are characteristic of posttraumatic stress disorder (PTSD). Given that impaired response inhibition is associated with worse symptom recovery and accumulating evidence pointing to the effectiveness of cognitive control trainings in reducing PTSD symptoms, individuals with moderate to severe PTSD total severity (Posttraumatic Diagnostic Scale total score ≥ 21) and pre-training response inhibition deficits (M ≤ 75% successful inhibition on the Go/No-go) completed a 3-h, adaptive Go/No-go training designed to improve ability to withhold prepotent motor responses. Then forty-nine participants were randomized to an adaptive response inhibition training (n = 24, M = 19.27 years, SD = 0.70) or a waitlist condition (n = 25, M = 18.31 years, SD = 4.80). Behavioral response inhibition and self-reported trauma-related symptoms were assessed at pre- and post-training. Response inhibition training was associated with improved response inhibition on an untrained transfer Stop-Signal task and symptom reduction in PTSD compared to a waitlist group, at post-training. There was, however, reduced inhibition on a modified Go/No-go task from pre-to post-training. Overall, response inhibition deficits and PTSD symptoms are amenable to top-down remediation using response inhibition training. Our study provides preliminary evidence for the feasibility of response inhibition training in a PTSD sample characterized by response inhibition deficits.
A review of burn symptoms and potential novel neural targets for non-invasive brain stimulation for treatment of burn sequelae
2021, Burns
Citation Excerpt :
The prefrontal area, similar as for other psychosocial dysregulation pathologies, plays a critical role. Indeed, the neural correlates of these psychiatric disorders, neuroimaging and lesion studies have identified the medial prefrontal cortex (mPFC) as one of the main structures involved [52–54]. More specifically, PTSD is thought to be linked to a dysregulated neurocircuit that mainly involves the amygdala, prefrontal regions, and hippocampus.
Burn survivors experience myriad associated symptoms such as pain, pruritus, fatigue, impaired motor strength, post-traumatic stress, depression, anxiety, and sleep disturbance. Many of these symptoms are common and remain chronic, despite current standard of care. One potential novel intervention to target these post burn symptoms is transcranial direct current stimulation (tDCS). tDCS is a non-invasive brain stimulation (NIBS) technique that modulates neural excitability of a specific target or neural network. The aim of this work is to review the neural circuits of the aforementioned clinical sequelae associated with burn injuries and to provide a scientific rationale for specific NIBS targets that can potentially treat these conditions. We ran a systematic review, following the PRISMA statement, of tDCS effects on burn symptoms. Only three studies matched our criteria. One was a feasibility study assessing cortical plasticity in chronic neuropathic pain following burn injury, one looked at the effects of tDCS to reduce pain anxiety during burn wound care, and one assessed the effects of tDCS to manage pain and pruritus in burn survivors. Current literature on NIBS in burn remains limited, only a few trials have been conducted. Based on our review and results in other populations suffering from similar symptoms as patients with burn injuries, three main areas were selected: the prefrontal region, the parietal area and the motor cortex. Based on the importance of the prefrontal cortex in the emotional component of pain and its implication in various psychosocial symptoms, targeting this region may represent the most promising target. Our review of the neural circuitry involved in post burn symptoms and suggested targeted areas for stimulation provide a spring board for future study initiatives.
Physical interventions for the treatment of trauma and stressor-related disorders: A comprehensive systematic review
2021, Mental Health and Physical Activity
Cognitive behavioral therapies for posttraumatic stress disorder (PTSD) are evidence-based and effective for many. However, the reach and impact of these interventions are limited. Physical interventions hold potential to bridge a gap in the unmet treatment of trauma and stressor-related disorders.
This systematic review examined 84 studies from four decades of research on physical interventions for trauma and stressor-related disorders to: 1) describe the state of the field and 2) summarize the best available evidence. Reviewed studies were described in terms of measured sample characteristics and assessed outcomes. Treatment effect patterns were analyzed by intervention content and study design.
The majority of studies (65.9%) reported statistically significant reductions in posttraumatic stress symptoms; 40.9% used a randomized controlled trial (RCT) design. Among RCTs, one performed rigorous, statistically powered analyses in an intention-to-treat sample.
High variability in reporting strategies among reviewed studies precludes analysis of variables such as intervention length, frequency, and dropout.
Preliminary evidence for the efficacy of physical interventions for trauma and stressor-related disorders is promising. Larger scale RCTs powered and designed to identify mediators and moderators of these interventions are warranted.

View all citing articles on Scopus

View full text

Original articleNeural Networks of Information Processing in Posttraumatic Stress Disorder: A Functional Magnetic Resonance Imaging Study

Background

Methods

Results

Conclusions

Section snippets

Participants

Reaction-Time Data

Clinical Data

Discussion

Biol Psychiatry

Biol Psychiatry

Biol Psychiatry

Biol Psychiatry

Biol Psychiatry

Trends Cogn Sci

Biol Psychiatry

Trends Cogn Sci

Biol Psychiatry

Biol Psychiatry

Behav Res Ther

Biol Psychiatry

Biol Psychiatry

Biol Psychiatry

Biol Psychology

Biol Psychiatry

Biol Psychiatry

Biol Psychiatry

Neuroimage

Biol Psychiatry

Neuroimage

The biology of being frazzled

Science

Neurobiology of decision-making: risk and reward

Sem Clin Neuropsychiat

A clinician rating scale for assessing current and lifetime PTSD: The CAPS-1

Behav Ther

Dorsal anterior cingulate cortex: A role in reward-based decision making

Proc Nat Acad Sci

The counting Stroop: an interference task specialized for functional neuroimaging – validation study with functional fMRI

Hum Brain Map

Original article
Neural Networks of Information Processing in Posttraumatic Stress Disorder: A Functional Magnetic Resonance Imaging Study