Neuroimaging in social anxiety disorder—A meta-analytic review resulting in a new neurofunctional model
Open accessAbstract
Social anxiety disorder (SAD) is one of the most frequent anxiety disorders. The landmark meta-analysis of functional neuroimaging studies by Etkin and Wager (2007) revealed primarily the typical fear circuit as overactive in SAD. Since then, new methodological developments such as functional connectivity and more standardized structural analyses of grey and white matter have been developed. We provide a comprehensive update and a meta-analysis of neuroimaging studies in SAD since 2007 and present a new model of the neurobiology of SAD. We confirmed the hyperactivation of the fear circuit (amygdala, insula, anterior cingulate and prefrontal cortex) in SAD. In addition, task-related functional studies revealed hyperactivation of medial parietal and occipital regions (posterior cingulate, precuneus, cuneus) in SAD and a reduced connectivity between parietal and limbic and executive network regions. Based on the result of this meta-analysis and review, we present an updated model of SAD adopting a network-based perspective. The disconnection of the medial parietal hub in SAD extends current frameworks for future research in anxiety disorders.
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The fusiform gyrus is central to visual face perception and meta-analyses show it is hyper-reactive to negative emotional stimuli in SAD.
“The fusiform gyrus plays a central role in visual face perception (McCarthy, Puce, Gore, & Allison, 1997), and has been shown in a meta-analyses to be hyper-reactive to negative emotional stimuli in social anxiety disorder (Brühl, Delsignore, et al., 2014; Etkin & Wager, 2007).”
From Changes in functional connectivity with cognitive behavioral therapy for social anxiety disorder predict outcomes at follow-up (2020) · cites this paper as Brühl, Delsignore, et al., 2014
The ALE meta-analysis (section 3.2, Table 3; page unavailable) finds greater fusiform gyrus activation in SAD than in healthy controls. Section 4.2 links this finding to feared negative facial expressions, but presents that explanation as a possibility; the meta-analysis does not establish that the increased response is specific to negative emotional stimuli. The face-perception clause is attributed to McCarthy et al., not to this source. (LLM, conf=0.85)
Experimental — accuracy not yet measuredAtypical recruitment of cortical regions, including dl/vl/mPFC and ACC, in SAD may be associated with emotion regulation deficits.
“Moreover, aberrant recruitment of cortical regions in SAD, including dorsolateral, ventrolateral, and medial prefrontal cortex (dl/vl/mPFC) and anterior cingulate cortex (ACC), may be linked to deficits in emotion regulation (Brühl, Delsignore, et al., 2014; Picó-Pérez, Radua, Steward, Menchón, & Soriano-Mas, 2017; Zilverstand, Parvaz, & Goldstein, 2017).”
From Changes in functional connectivity with cognitive behavioral therapy for social anxiety disorder predict outcomes at follow-up (2020) · cites this paper as Brühl, Delsignore, et al., 2014
Neurobiological models propose that prefrontal cortex regions regulate emotional reactivity in the amygdala through top-down connectivity.
“Neurobiological models suggest that regions of the prefrontal cortex (PFC) are central to regulation of emotional reactivity in the amygdala through top-down connectivity (Berkman & Lieberman, 2009; Brühl, Delsignore, Komossa, & Weidt, 2014).”
From Changes in functional connectivity with cognitive behavioral therapy for social anxiety disorder predict outcomes at follow-up (2020) · cites this paper as Brühl, Delsignore, Komossa, & Weidt, 2014
Prior findings disagree about which prefrontal subregions are involved and whether activation is increased or decreased relative to healthy controls.
“However, findings have been inconsistent regarding the specific prefrontal sub-regions as well as direction of effects (both relatively increased (Brühl, Delsignore, et al., 2014; Goldin et al., 2009) or decreased activation (Zilverstand et al., 2017) compared to healthy individuals).”
From Changes in functional connectivity with cognitive behavioral therapy for social anxiety disorder predict outcomes at follow-up (2020) · cites this paper as Brühl, Delsignore, et al., 2014
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Gold, A. L., Shechner, T., Farber, M. J., Spiro, C. N., Leibenluft, E., Pine, D. S., & Britton, J. C. (2016) · Depression and Anxiety · doi:10.1002/da.22470 · Cited by 82 · see citing works
Young, K. S., Burklund, L. J., Torre, J. B., Saxbe, D., Lieberman, M. D., & Craske, M. G. (2017) · Psychiatry Research - Neuroimaging · doi:10.1016/j.pscychresns.2017.01.005 · Cited by 64 · see citing works
“…with SAD, relative to healthy control participants when explicitly instructed to engage in a regulatory strategy (for recent meta-analyses, see Brühl et al., 2014; Zilverstand http://dx.doi.org/10.1016/j.pscychresns.2017.01.005 Received 9 September 2016; Received in revised form 5 January…”
BackgroundInfluentialKlumpp, H., Fitzgerald, J. M., Kinney, K. L., Kennedy, A. E., Shankman, S. A., Langenecker, S. A., & Phan, K. L. (2017) · NeuroImage: Clinical · doi:10.1016/j.nicl.2017.04.006 · Cited by 59 · see citing works
Neuromarkers for Mental Disorders: Harnessing Population Neuroscience
Jollans, L., & Whelan, R. (2018) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2018.00242 · Cited by 56 · see citing works
Atypical amygdala response to fear conditioning in autism spectrum disorder
Top Jr., D. N., Stephenson, K. G., Doxey, C. R., Crowley, M. J., Kirwan, C. B., & South, M. (2016) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2016.01.008 · Cited by 45 · see citing works
Gingnell, M., Frick, A., Engman, J., Alaie, I., Björkstrand, J., Faria, V., Carlbring, P., Andersson, G., Reis, M., Larsson, E.-M., et al. (2016) · British Journal of Psychiatry · doi:10.1192/bjp.bp.115.175794 · Cited by 44 · see citing works
Nagata, T., Suzuki, F., & Teo, A. R. (2015) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12327 · Cited by 40 · see citing works
Burklund, L. J., Torre, J. B., Lieberman, M. D., Taylor, S. E., & Craske, M. G. (2017) · Psychiatry Research - Neuroimaging · doi:10.1016/j.pscychresns.2016.12.012 · Cited by 38 · see citing works
Neural effects of a short-term virtual reality self-training program to reduce social anxiety
Kim, M.-K., Eom, H., Kwon, J. H., Kyeong, S., & Kim, J.-J. (2022) · Psychological Medicine · doi:10.1017/s0033291720003098 · Cited by 36 · see citing works
Vulnerabilities in social anxiety: Integrating intra- and interpersonal perspectives
Ginat-Frolich, R., Gilboa-Schechtman, E., Huppert, J. D., Aderka, I. M., Alden, L. E., Bar-Haim, Y., Becker, E. S., Bernstein, A., Geva, R., Heimberg, R. G., et al. (2024) · Clinical Psychology Review · doi:10.1016/j.cpr.2024.102415 · Cited by 36 · see citing works
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“The neurobiological model of emotion regulation states that reactivity to emotional stimuli in the amygdala is regulated through top-down connectivity with regions of the prefrontal cortex (PFC; Brühl et al., 2014; Goldin et al., 2009b; Ochsner and Gross, 2005; Zilverstand et al., 2016; Ziv et al., 2013).”
A voice without a mouth no more: The neurobiology of language and consciousness
Skipper, J. I. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104772 · Cited by 31 · see citing works
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Weidt, S., Lutz, J., Rufer, M., Delsignore, A., Jakob, N. J., Herwig, U., & Bruehl, A. B. (2016) · Psychological Medicine · doi:10.1017/s0033291715002998 · Cited by 30 · see citing works
Self-citationBrown, L. A., Young, K. S., Goldin, P. R., Torre, J. B., Burklund, L. J., Davies, C. D., Niles, A. N., Lieberman, M. D., Saxbe, D. E., & Craske, M. G. (2019) · Psychiatry Research - Neuroimaging · doi:10.1016/j.pscychresns.2018.12.017 · Cited by 24 · see citing works
“The threat-detection neural circuitry underlying fears of negative evaluation involves the amygdala, precuneus, insula, anterior cingulate, and prefrontal cortices (Brühl et al, 2014; Etkin and Wager, 2007).”
BackgroundAltered time course of amygdala activation during speech anticipation in social anxiety disorder
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“Neurobiological models suggest that regions of the prefrontal cortex (PFC) are central to regulation of emotional reactivity in the amygdala through top-down connectivity (Berkman and Lieberman, 2009; Brühl, Delsignore, Komossa, and Weidt, 2014).”
BackgroundInfluentialFrick, A., Åhs, F., Appel, L., Jonasson, M., Wahlstedt, K., Bani, M., Merlo Pich, E., Bettica, P., Långström, B., Lubberink, M., et al. (2016) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2016.09.004 · Cited by 22 · see citing works
Resting functional connectivity in social anxiety disorder and the effect of pharmacotherapy
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Lukow, P. B., Lowther, M., Pike, A. C., Yamamori, Y., Chavanne, A. V., Gormley, S., Aylward, J., McCloud, T., Goble, T., Rodriguez-Sanchez, J., et al. (2024) · Journal of Psychopharmacology · doi:10.1177/02698811241286773 · Cited by 3 · see citing works
“Both their activation and connectivity are associated with anxiety (Brühl et al., 2014; Carlisi and Robinson, 2018; Chavanne and Robinson, 2021; Etkin and Wager, 2007; Freitas-Ferrari et al., 2010; Goossen et al., 2019; Hattingh et al., 2012; Ipser et al., 2013; Kalisch and Gerlicher, 2014;…”
Background
- Authors
- Brühl, A. B., Delsignore, A., Komossa, K., & Weidt, S.
- Affiliations
- University of Zurich (CH)
- University Hospital Zurich (CH)
- Corresponding author
- Brühl, Annette Beatrix
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2014-11
- Volume
- 47
- Pages
- 260-280
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W1993400322
- Cited by
- 439
- References
- 62
- Citations by year
- 2026: 16 · 2025: 34 · 2024: 107 · 2023: 30 · 2022: 29 · 2021: 29 · 2020: 31 · 2019: 32 · 2018: 36 · 2017: 30 · 2016: 42 · 2015: 19 · 2014: 3
- FWCI
- 4.25
- Type
- journal article
- Language
- en
- Open access
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Topics
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- social anxiety disorder, fear circuit, amygdala, insula, anterior cingulate cortex, prefrontal cortex, posterior cingulate cortex, precuneus, cuneus, functional connectivity, network models
- MeSH terms
- Brain, Brain Mapping, Humans, Models, Neurological, Phobic Disorders, Neuroimaging
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