Paradoxical Prefrontal–Amygdala Recruitment to Angry and Happy Expressions in Pediatric Posttraumatic Stress Disorder
Open accessAbstract
The neural substrates of pediatric posttraumatic stress disorder (PTSD) remain incompletely understood, but likely involve abnormal function and development of emotion processing circuitry. Valence-specific and age-related abnormalities during emotion processing have not been elucidated. We examined implicit emotional face processing in pediatric PTSD, predicting abnormalities specific to threat-related emotion. Youth (ages 8-18 years) with PTSD (n=25) and healthy youth (n=28) completed a dynamic emotional face task during fMRI, viewing faces changing from neutral to angry or happy, or changing shape control. Group and cross-sectional age-related differences in activation and functional connectivity were examined in amygdala/hippocampus, medial prefrontal cortex (mPFC), and whole-brain analyses. The post hoc analyses examined the relationship of neural abnormalities with symptom measures of PTSD, anxiety, and depression. Compared with decreased activation with age in healthy youth, PTSD youth showed increased amygdala activation to emotional faces with age. In a group by emotion interaction, PTSD youth showed dorsal (d)ACC hyperactivation to happy faces relative to healthy youth, with no difference for angry faces. Connectivity analyses revealed paradoxical coupling in prefrontal-amygdala circuits, including dACC-dorsomedial (dm)PFC, amygdala-dmPFC, and amygdala-ventrolateral (vl)PFC. In each case, PTSD youth showed reduced connectivity to angry faces, but increased connectivity to happy faces, the reverse of healthy youth. Valence-abnormal recruitment was associated with greater symptom severity, implicating a role in trauma-related psychopathology in youth. Notably, impaired recruitment during angry faces and heightened recruitment to happy faces may reflect increased salience and ambiguity of positive emotional expressions in pediatric PTSD. Finally, age-related findings suggest a developmental sensitization of the amygdala across emotional expressions in youth with PTSD. These findings provide novel insights into the underlying pathophysiology of pediatric PTSD, extending beyond abnormal neural responses to canonical threat.
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Amygdala activation is lower in PTSD compared to TD youth at younger ages (<15 years), but hyperactive by late adolescence.
“amygdala activation was actually lower in PTSD compared to TD youth at younger ages (<15 years), but showed hyperactivation by late adolescence.”
From Trauma, PTSD, and the Developing Brain (2017) · cites this paper as [35]
The Regional Brain Activation results report that right-amygdala activation decreased with age in healthy youth but increased with age in youth with PTSD; the Discussion describes the same pattern. Our copy does not establish the claimed below-15 cutoff or explicitly report lower activation in the younger PTSD group and hyperactivation relative to controls by late adolescence. (LLM, conf=0.83)
Experimental — accuracy not yet measuredPediatric PTSD is associated with a failure to upregulate prefrontal circuits and increasing amygdala reactivity with age.
“recent neuroimaging studies of pediatric PTSD suggest a failure to upregulate prefrontal circuits, but nevertheless show increasing amygdala reactivity with age.”
From Trauma, PTSD, and the Developing Brain (2017) · cites this paper as [35]
The Discussion reports increasing amygdala activation with age in youth with PTSD. It also reports decreased recruitment of prefrontal emotion-regulatory circuits to angry faces, but heightened recruitment to happy faces. Thus, a general failure to upregulate prefrontal circuits omits an important condition-specific finding. (LLM, conf=0.88)
Experimental — accuracy not yet measuredYouth with PTSD exhibit reduced coupling between amygdala and rACC/dmPFC, which is linked to PTSD severity.
“we found that youth with PTSD exhibit reduced coupling between the amygdala and rACC/dmPFC, which was further linked to PTSD severity [35,57].”
From Trauma, PTSD, and the Developing Brain (2017) · cites this paper as [35]
The Functional Connectivity section reports reduced amygdala–dmPFC connectivity in youth with PTSD for angry faces, but increased connectivity for happy faces. It links this connectivity to hyperarousal symptoms, although the negative correlation for angry faces was only a trend. The passages do not establish reduced amygdala–rACC coupling; rACC connectivity results are said to be in supplementary material. (LLM, conf=0.87)
Experimental — accuracy not yet measuredIn TD youth, amygdala reactivity to negative faces and images decreases with age, accompanied by greater structural and functional connectivity between amygdala and mPFC/rACC.
“amygdala reactivity to negative faces and images decreases with age [21,33–36], and is accompanied by greater structural and functional connectivity between the amygdala and mPFC/rACC [25,33,34,36].”
From Trauma, PTSD, and the Developing Brain (2017) · cites this paper as [35]
The Regional Brain Activation results (page unavailable) report that amygdala activation decreased with age in healthy youth, but the finding was across angry and happy face conditions, not specifically negative stimuli. The Functional Connectivity results describe responses to angry versus happy faces, not age-related increases in connectivity; the paper does not report structural connectivity or responses to negative images in these healthy youth. (LLM, conf=0.88)
Experimental — accuracy not yet measuredAge-related findings in pediatric PTSD were not accounted for by age at index trauma or duration of PTSD.
“our age-related findings in pediatric PTSD (e.g. increased amygdala activation, decreased amygdala-vmPFC coupling with age) were not accounted for by age at index trauma or duration of PTSD [35,53,57].”
From Trauma, PTSD, and the Developing Brain (2017) · cites this paper as [35]
The Discussion reports that age-related findings in the PTSD group remained after adjustment for illness duration and time elapsed since index trauma. Time elapsed since trauma is not age at trauma, and the Introduction describes decreased amygdala–vmPFC connectivity with age as a finding from a prior study, not a finding tested here against those covariates. (LLM, conf=0.87)
Experimental — accuracy not yet measured
Youth with PTSD show increasing amygdala reactivity with age.
“increasing amygdala reactivity”
From Trauma, PTSD, and the Developing Brain (2017) · cites this paper as [35]
In pediatric PTSD, there is a group by age interaction on amygdala activation to angry and happy faces: TD youth show decreased activation with age, while youth with PTSD show increased activation with age.
“we found a group by age interaction on amygdala activation to both angry and happy faces. Specifically, TD youth showed the expected pattern of decreased amygdala activation with age, while youth with PTSD showed increased activation with age [35].”
From Trauma, PTSD, and the Developing Brain (2017) · cites this paper as [35]
Prefrontal-cingulate findings during emotion processing in pediatric PTSD are mixed.
“Prefrontal-cingulate findings during emotion processing in pediatric PTSD have largely been mixed to date.”
From Trauma, PTSD, and the Developing Brain (2017) · cites this paper as [35]
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References 62 · Cited by 60
- Authors
- Keding, T. J., & Herringa, R. J.
- Affiliations
- University of Wisconsin–Madison (US)
- Corresponding author
- Herringa, Ryan J
- Venue
- Neuropsychopharmacology
- Published
- 2016-06-22
- Volume
- 41
- Issue
- 12
- Pages
- 2903-2912
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC5061882
- OpenAlex
- W2473926707
- Cited by
- 60
- References
- 62
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 3 · 2023: 6 · 2022: 10 · 2021: 6 · 2020: 10 · 2019: 6 · 2018: 9 · 2017: 1 · 2016: 1
- FWCI
- 7.59
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- National Institutes of Health (UL1TR000427, NIH/NCATS UL1 TR000427)
- Institute for Clinical and Translational Research, University of Wisconsin, Madison (NIH/NCATS UL1TR000427, UL1TR000427)
- School of Medicine and Public Health, University of Wisconsin-Madison (UL1‐TR‐000427)
- National Institute of Mental Health (MH100267, K08MH100267)
- National Center for Advancing Translational Sciences (NCATS UL1TR000427)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
- Keywords
- emotional face processing, amygdala, medial prefrontal cortex, anterior cingulate cortex, amygdala hyperactivation, anxiety and depressive symptoms
- MeSH terms
- Adolescent, Amygdala, Anger, Child, Cross-Sectional Studies, Face, Female, Happiness, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Neural Pathways, Oxygen, Photic Stimulation, Psychiatric Status Rating Scales, Psychophysics, Stress Disorders, Post-Traumatic, Prefrontal Cortex
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