Disrupted amygdalar subregion functional connectivity and evidence of a compensatory network in generalized anxiety disorder
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CONTEXT: Little is known about the neural abnormalities underlying generalized anxiety disorder (GAD). Studies in other anxiety disorders have implicated the amygdala, but work in GAD has yielded conflicting results. The amygdala is composed of distinct subregions that interact with dissociable brain networks, which have been studied only in experimental animals. A functional connectivity approach at the subregional level may therefore yield novel insights into GAD. OBJECTIVES: To determine whether distinct connectivity patterns can be reliably identified for the basolateral (BLA) and centromedial (CMA) subregions of the human amygdala, and to examine subregional connectivity patterns and potential compensatory amygdalar connectivity in GAD. DESIGN: Cross-sectional study. SETTING: Academic medical center. PARTICIPANTS: Two cohorts of healthy control subjects (consisting of 17 and 31 subjects) and 16 patients with GAD. MAIN OUTCOME MEASURES: Functional connectivity with cytoarchitectonically determined BLA and CMA regions of interest, measured during functional magnetic resonance imaging performed while subjects were resting quietly in the scanner. Amygdalar gray matter volume was also investigated with voxel-based morphometry. RESULTS: Reproducible subregional differences in large-scale connectivity were identified in both cohorts of healthy controls. The BLA was differentially connected with primary and higher-order sensory and medial prefrontal cortices. The CMA was connected with the midbrain, thalamus, and cerebellum. In GAD patients, BLA and CMA connectivity patterns were significantly less distinct, and increased gray matter volume was noted primarily in the CMA. Across the subregions, GAD patients had increased connectivity with a previously characterized frontoparietal executive control network and decreased connectivity with an insula- and cingulate-based salience network. CONCLUSIONS: Our findings provide new insights into the functional neuroanatomy of the human amygdala and converge with connectivity studies in experimental animals. In GAD, we find evidence of an intra-amygdalar abnormality and engagement of a compensatory frontoparietal executive control network, consistent with cognitive theories of GAD.
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Relative to healthy controls, GAD patients have stronger resting-state connectivity among the amygdala, vmPFC, and dlPFC, and this coupling increases with anxiety severity.
“Etkin, Prater, Schatzberg, Menon, and Greicius (2009) found that generalized anxiety disorder (GAD) patients, as compared to healthy control participants, evidenced stronger resting state connectivity between the amygdala, the ventromedial PFC, and the dorsolateral PFC, and this connectivity was stronger as a function of anxiety severity.”
From What, me worry and ruminate about dsm-5 and rdoc? The importance of targeting negative self-referential processing (2013) · cites this paper as Etkin et al., 2009
The Comment section reports increased amygdala connectivity with both the ventromedial and dorsolateral PFC in GAD patients. But the Results section reports that amygdala–DLPFC connectivity was negatively correlated with all anxiety measures: it was strongest in the least anxious patients, contrary to the claimed increase with anxiety severity. Page numbers are not available in our copy. (LLM, conf=0.91)
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Experimental — accuracy not yet measuredIncreased functional VLPFC-amygdala connectivity in emotion acceptance is in contrast to reduced VLPFC-amygdala connectivity found in GAD more generally.
“However, the increased functional VLPFC-amygdala connectivity in emotion acceptance is in contrast to reduced VLPFC-amygdala connectivity found in GAD more generally (Monk et al., 2008; Etkin et al., 2009).”
From Neural correlates of emotion acceptance<i>vs</i>worry or suppression in generalized anxiety disorder (2017) · cites this paper as Etkin et al., 2009
The Comment section (page unavailable) reports decreased ventrolateral PFC–amygdala connectivity in patients with GAD, supporting the cited contrast. But it also reports increased connectivity with ventrolateral PFC in a different network, so the paper does not support an unqualified characterization of VLPFC–amygdala connectivity in GAD as reduced. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThe association between VLPFC activation and distress ratings in worry and emotion suppression is consistent with the role of the VLPFC in reflexive reorienting and with existing studies of GAD, in which VLPFC recruitment may represent maladaptive or compensatory activation necessary to regulate worry-related anxiety.
“The association between VLPFC activation and distress ratings in worry and emotion suppression are consistent with the role of the VLPFC in reflexive reorienting discussed earlier and with existing studies of GAD, in which VLPFC recruitment may represent maladaptive or compensatory activation necessary to regulate worry-related anxiety (Monk et al., 2008; Etkin et al., 2009).”
From Neural correlates of emotion acceptance<i>vs</i>worry or suppression in generalized anxiety disorder (2017) · cites this paper as Etkin et al., 2009
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Experimental — accuracy not yet measuredfMRI studies of worry have shown reduced amygdala-VLPFC connectivity in GAD.
“and reduced amygdala-VLPFC connectivity in GAD (Monk et al., 2008; Etkin et al., 2009)”
From Neural correlates of emotion acceptance<i>vs</i>worry or suppression in generalized anxiety disorder (2017) · cites this paper as Etkin et al., 2009
The findings are consistent with prior reports implicating the CeA in anxiety.
“These data are consistent with reports implicating CeA involvement in anxiety9,11,12”
From Amygdala circuitry mediating reversible and bidirectional control of anxiety (2011) · cites this paper as [11]
Resting-state amygdala connectivity has been reported to be altered in individuals with generalized anxiety disorder, social phobia, major depressive disorder and bipolar disorder.
“it has been reported to be altered in individuals with generalized anxiety disorder (GAD),39 social phobia,40 major depressive disorder (MDD)41,42 and bipolar disorder;43”
From Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder (2012) · cites this paper as [39]
The neural systems implicated in anxiety by rodent studies are consistent with those identified in human patients.
“This contrast notwithstanding, the neural systems implicated in anxiety by rodent studies are consistent with those identified in human patients26-34, underscoring the utility and translatability of these rodent studies.”
From Resolving the neural circuits of anxiety (2015) · cites this paper as [29]
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“Consistent with Borkovec and colleagues' (2004) view that worry serves to help reduce distress caused by emotional arousal, Etkin et al. (2009) interpreted the role of the dorsolateral prefrontal cortex (DLPFC) here as a form of compensatory, but not necessarily optimal, neural adaptation.”
BackgroundOxytocin׳s role in anxiety: A critical appraisal
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“Despite these considerations, cytoarchitechtonically based amygdala FC analyses have yielded consistent, replicated delineation of differential connectivity of major amygdala subregions (Etkin et al., 2009; Roy et al., 2009; Roy et al., 2013; Brown et al., 2014 ).”
InfluentialImmature integration and segregation of emotion-related brain circuitry in young children
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“recently reported abnormal amygdala-lateral PFC coupling.[17] As the lateral PFC–amygdala connectivity was strongest in the least anxious subjects, the authors suggested a compensatory role for the lateral PFC in the cognitive regulation of emotion in GAD.”
BackgroundResultInfluentialAmygdala NRG1–ErbB4 Is Critical for the Modulation of Anxiety-Like Behaviors
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“The association between VLPFC activation and distress ratings in worry and emotion suppression are consistent with the role of the VLPFC in reflexive reorienting discussed earlier and with existing studies of GAD, in which VLPFC recruitment may represent maladaptive or compensatory activation necessary to regulate wor…”
BackgroundResultInfluentialChanges in functional connectivity following treatment with emotion regulation therapy
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Personalized Clinical Approaches to Anxiety Disorders
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- Authors
- Etkin, A., Prater, K. E., Schatzberg, A. F., Menon, V., & Greicius, M. D.
- Affiliations
- Stanford Medicine (US)
- Venue
- Archives of General Psychiatry
- Publisher
- American Medical Association (AMA)
- Published
- 2009-12-01
- Volume
- 66
- Issue
- 12
- Pages
- 1361
- ISSN
- 0003-990X (ISSN-L)
- PMC
- PMC12553334
- OpenAlex
- W2156874786
- Semantic Scholar
- 6fa2fa52c02a7364ed7d3dea499112ffff6364b4
- Cited by
- 664
- References
- 79
- Citations by year
- 2026: 19 · 2025: 32 · 2024: 31 · 2023: 34 · 2022: 40 · 2021: 38 · 2020: 40 · 2019: 62 · 2018: 41 · 2017: 51 · 2016: 55 · 2015: 44 · 2014: 44 · 2013: 46 · 2012: 32
- FWCI
- 13.76
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Archives of General Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (K23NS048302, NS048302, NS058899, R21NS058899)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD047520, R01HD047520)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- generalized anxiety disorder, amygdala, basolateral amygdala, centromedial amygdala, functional connectivity, salience network, resting-state functional connectivity
- MeSH terms
- Adult, Amygdala, Anxiety Disorders, Auditory Cortex, Brain, Brain Mapping, Cross-Sectional Studies, Female, Frontal Lobe, Humans, Magnetic Resonance Imaging, Male, Nerve Net, Neural Pathways, Parietal Lobe, Personality Inventory, Psychiatric Status Rating Scales, Surveys and Questionnaires, Cohort Studies, Prefrontal Cortex
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