Differential patterns of activity and functional connectivity in emotion processing neural circuitry to angry and happy faces in adolescents with and without suicide attempt
Open accessAbstract
BACKGROUND: Neural substrates of emotion dysregulation in adolescent suicide attempters remain unexamined. METHOD: We used functional magnetic resonance imaging to measure neural activity to neutral, mild or intense (i.e., 0%, 50% or 100% intensity) emotion face morphs in two separate emotion-processing runs (angry and happy) in three adolescent groups: (1) history of suicide attempt and depression (ATT, n=14) ; (2) history of depression alone (NAT, n=15) ; and (3) healthy controls (HC, n=15). Post-hoc analyses were conducted on interactions from 3 group x 3 condition (intensities) whole-brain analyses (p<0.05, corrected) for each emotion run. RESULTS: To 50% intensity angry faces, ATT showed significantly greater activity than NAT in anterior cingulate gyral–dorsolateral prefrontal cortical attentional control circuitry, primary sensory and temporal cortices; and significantly greater activity than HC in the primary sensory cortex, while NAT had significantly lower activity than HC in the anterior cingulate gyrus and ventromedial prefrontal cortex. To neutral faces during the angry emotion processing run, ATT had significantly lower activity than NAT in the fusiform gyrus. ATT also showed significantly lower activity than HC to 100% intensity happy faces in the primary sensory cortex, and to neutral faces in the happy run in the anterior cingulate and left medial frontal gyri (all p<0.006,corrected). Psychophysiological interaction analyses revealed significantly reduced anterior cingulate gyral–insula functional connectivity to 50% intensity angry faces in ATT v. NAT or HC. CONCLUSIONS: Elevated activity in attention control circuitry, and reduced anterior cingulate gyral–insula functional connectivity, to 50% intensity angry faces in ATT than other groups suggest that ATT may show inefficient recruitment of attentional control neural circuitry when regulating attention to mild intensity angry faces, which may represent a potential biological marker for suicide risk.
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Individuals with a history of suicidal ideation or behavior show altered neural activation and neural network connectivity in prefrontal cortex regions.
“An emerging line of research points to altered neural activation (Just et al. 2017, Miller et al. 2018, Pan et al. 2013, Quevedo et al. 2016) and neural network connectivity (Chase et al. 2017; Ordaz et al. 2018; Zhang et al. 2014, 2016) in PFC regions among individuals with a history of suicidal ideation or behavior.”
From Adolescent Suicide as a Failure of Acute Stress-Response Systems. (2019) · cites this paper as Pan et al. 2013
Depressed attempters show reduced connectivity between a right ACC seed and bilateral insula when viewing 50% angry faces versus baseline relative to depressed non-attempters and healthy controls.
“Group differences in PPI show reduced connectivity between a right ACC seed and the bilateral insula when viewing 50% angry faces versus baseline for depressed attempters relative to depressed non-attempters and healthy controls.”
From Neural correlates associated with suicide and nonsuicidal self-injury in youth (2021) · cites this paper as [83]
During the 50% angry face condition, attempters show greater activation in attentional control circuitry (right ACC, left DLPFC), primary sensory cortex, and right middle temporal gyrus relative to non-attempters.
“relative to non-attempters, attempters show greater activation in attentional control circuitry (right ACC, left DLPFC), primary sensory cortex, and right middle temporal gyrus (83).”
From Neural correlates associated with suicide and nonsuicidal self-injury in youth (2021) · cites this paper as [83]
Suicide attempters have less OFC and rACC activity in response to positive facial expressions and greater lateral OFC activity in response to angry facial expressions.
“Suicide attempters also have less OFC and rACC activity in response to positive facial expressions (78) and greater lateral OFC activity in response to angry facial expressions (95, 97, 104).”
From A brain-centric model of suicidal behavior (2020) · cites this paper as [97]
Compared with suicide nonattempters, suicide attempters with the same diagnosis show less activity in the dlPFC, rACC, dACC, thalamus, and insula during decision-making tasks.
“Compared with suicide nonattempters, suicide attempters having the same diagnosis manifest less activity in the dlPFC, rACC, dACC, thalamus, and insula while performing decision-making tasks (e.g., the Iowa Gambling Task) (95-99).”
From A brain-centric model of suicidal behavior (2020) · cites this paper as [97]
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Functional imaging of the implicit association of the self with life and death
Ballard, E. D., Reed, J. L., Szczepanik, J., Evans, J. W., Yarrington, J. S., Dickstein, D. P., Nock, M. K., Nugent, A. C., & Zarate, C. A. (2019) · Suicide and Life-Threatening Behavior · doi:10.1111/sltb.12543 · Cited by 22 · see citing works
- Authors
- Pan, L. A., Hassel, S., Segreti, A. M., Nau, S. A., Brent, D. A., & Phillips, M. L.
- Affiliations
- University of Pittsburgh (US)
- University of Calgary (CA)
- Corresponding author
- Pan, L. A.
- Venue
- Psychological Medicine
- Publisher
- Cambridge University Press (CUP)
- Published
- 2013-01-09
- Volume
- 43
- Issue
- 10
- Pages
- 2129-2142
- ISSN
- 0033-2917 (ISSN-L)
- 1469-8978
- OpenAlex
- W2161993030
- Cited by
- 183
- References
- 45
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 8 · 2023: 9 · 2022: 17 · 2021: 19 · 2020: 16 · 2019: 16 · 2018: 30 · 2017: 11 · 2016: 15 · 2015: 9 · 2014: 14 · 2013: 1
- FWCI
- 14.46
- Type
- journal article
- Language
- en
- Open access
- Locations
- Psychological Medicine (publishedVersion)
- PubMed (publishedVersion)
- Aston Publications Explorer (Aston University) (submittedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (submittedVersion)
- Funders
- American Foundation for Suicide Prevention
- University of Pittsburgh
- Carnegie Mellon University
- National Institutes of Health (5r01mh076971-05)
- National Institute of Mental Health (MH076971, -MH56612, MH-18951, -MH65368, K23MH082884, U10MH066775, R01MH065368, MH66775, T32MH018951)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Suicide and Self-Harm Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Keywords
- adolescent suicide attempts, emotional dysregulation, anger, happiness, functional connectivity, anterior cingulate cortex, insula, attentional control, ventromedial prefrontal cortex, fusiform gyrus, depression, emotional intensity
- MeSH terms
- Adolescent, Anger, Attention, Cerebral Cortex, Major Depressive Disorder, Depressive Disorder, Major, Emotions, Facial Expression, Female, Gyrus Cinguli, Happiness, Humans, Magnetic Resonance Imaging, Male, Somatosensory Cortex, Suicide, Attempted, Biomarkers, Prefrontal Cortex, Connectome
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