Neural mechanisms underlying heterogeneity in the presentation of anxious temperament
Open accessAbstract
Children with an anxious temperament (AT) are at risk for developing psychiatric disorders along the internalizing spectrum, including anxiety and depression. Like these disorders, AT is a multidimensional phenotype and children with extreme anxiety show varying mixtures of physiological, behavioral, and other symptoms. Using a well-validated juvenile monkey model of AT, we addressed the degree to which this phenotypic heterogeneity reflects fundamental differences or similarities in the underlying neurobiology. The rhesus macaque is optimal for studying AT because children and young monkeys express the anxious phenotype in similar ways and have similar neurobiology. Fluorodeoxyglucose (FDG)-positron emission tomography (FDG-PET) in 238 freely behaving monkeys identified brain regions where metabolism predicted variation in three dimensions of the AT phenotype: hypothalamic-pituitary-adrenal (HPA) activity, freezing behavior, and expressive vocalizations. We distinguished brain regions that predicted all three dimensions of the phenotype from those that selectively predicted a single dimension. Elevated activity in the central nucleus of the amygdala and the anterior hippocampus was consistently found across individuals with different presentations of AT. In contrast, elevated activity in the lateral anterior hippocampus was selective to individuals with high levels of HPA activity, and decreased activity in the motor cortex (M1) was selective to those with high levels of freezing behavior. Furthermore, activity in these phenotype-selective regions mediated relations between amygdala metabolism and different expressions of anxiety. These findings provide a framework for understanding the mechanisms that lead to heterogeneity in the clinical presentation of internalizing disorders and set the stage for developing improved interventions.
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The central nucleus can initiate a broad spectrum of defensive responses through efferent projections to brain regions that directly mediate behavioral, physiological, and cognitive features of anxiety.
“the Ce can initiate a broad spectrum of defensive responses via efferent projections to the brain regions that directly mediate many of the behavioral, physiological, and cognitive features of anxiety11, 18-19.”
From Evolutionarily conserved prefrontal-amygdalar dysfunction in early-life anxiety (2014) · cites this paper as [11]
In young monkeys, individual differences in central nucleus metabolism are trait-like and predict substantial variation in anxious temperament.
“in young monkeys individual differences in Ce metabolism are trait-like and predict substantial variation in the AT phenotype10-13.”
From Evolutionarily conserved prefrontal-amygdalar dysfunction in early-life anxiety (2014) · cites this paper as [11]
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Birn, R. M., Shackman, A. J., Oler, J. A., Williams, L. E., McFarlin, D. R., Rogers, G. M., Shelton, S. E., Alexander, A. L., Pine, D. S., Slattery, M. J., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.46 · Cited by 159 · see citing works
Self-citationFailure to filter: Anxious individuals show inefficient gating of threat from working memory
Stout, D. M., Shackman, A. J., & Larson, C. L. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00058 · Cited by 133 · see citing works
Self-citationVisser, R. M., Kunze, A. E., Westhoff, B., Scholte, H. S., & Kindt, M. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.01.021 · Cited by 52 · see citing works
Prefrontal Regulation of Threat-Elicited Behaviors: A Pathway to Translation
Roberts, A. C. (2020) · Annual Review of Psychology · doi:10.1146/annurev-psych-010419-050905 · Cited by 50 · see citing works
Cremers, H. R., Veer, I. M., Spinhoven, P., Rombouts, S. A. R. B., Yarkoni, T., Wager, T. D., & Roelofs, K. (2015) · Psychological Medicine · doi:10.1017/s0033291714002657 · Cited by 38 · see citing works
Nelson, B. D., Liu, H., Sarapas, C., & Shankman, S. A. (2016) · Journal of Experimental Psychopathology · doi:10.5127/jep.048115 · Cited by 32 · see citing works
- Authors
- Shackman, A. J., Fox, A. S., Oler, J. A., Shelton, S. E., Davidson, R. J., & Kalin, N. H.
- Affiliations
- Department of Psychiatry,
- University of Wisconsin–Madison (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-03-28
- Volume
- 110
- Issue
- 15
- Pages
- 6145-6150
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3625282
- OpenAlex
- W2163421192
- Cited by
- 113
- References
- 93
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 7 · 2023: 11 · 2022: 5 · 2021: 9 · 2020: 11 · 2019: 8 · 2018: 8 · 2017: 8 · 2016: 16 · 2015: 9 · 2014: 11 · 2013: 3
- FWCI
- 17.57
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (RR000167, MH084051, HD003352, P51OD011106)
- National Institute of Mental Health (MH084051, MH046729, R21MH091550, MH018931, MH081884, MH091550, P50MH084051, R01MH043454, R01MH046729, T32MH018931, R01MH081884)
- National Center for Research Resources (RR 000167, P51RR000167)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD003352, HD003352, F32HD008352, HD008352)
- Topics
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- anxious temperament, phenotypic heterogeneity, rhesus monkeys, brain glucose metabolism, central amygdala, anterior hippocampus, freezing behavior, vocalizations, motor cortex, internalizing disorders, anxiety, depression
- MeSH terms
- Amygdala, Animals, Anxiety, Brain, Brain Mapping, Depression, False Positive Reactions, Female, Hippocampus, Hydrocortisone, Macaca mulatta, Male, Models, Neurological, Phenotype, Radioimmunoassay, Time Factors, Models, Animal, Neuroimaging
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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