Uncertainty during anticipation modulates neural responses to aversion in human insula and amygdala

Sarinopoulos, I.; Grupe, D. W.; Mackiewicz, K. L.; Herrington, J. D.; Lor, M.; Steege, E. E.; Nitschke, J. B.

doi:10.1093/cercor/bhp155

Cited by 241Neural and Behavioral Psychology StudiesMemory and Neural MechanismsAnxiety, Depression, Psychometrics, Treatment, Cognitive Processes

Uncertainty during anticipation modulates neural responses to aversion in human insula and amygdala

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Sarinopoulos, I., Grupe, D. W., Mackiewicz, K. L., Herrington, J. D., Lor, M., Steege, E. E., Nitschke, J. B.·2010·Cerebral Cortex

DOI 10.1093/cercor/bhp155PMC PMC2837092

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Abstract

Uncertainty about potential negative future outcomes can cause stress and is a central feature of anxiety disorders. The stress and anxiety associated with uncertain situations may lead individuals to overestimate the frequency with which uncertain cues are followed by negative outcomes, an example of covariation bias. Using functional magnetic resonance imaging, we found that uncertainty-related expectations modulated neural responses to aversion. Insula and amygdala responses to aversive pictures were larger after an uncertain cue (that preceded aversive or neutral pictures) than a certain cue (that always preceded aversive pictures). Anticipatory anterior cingulate cortex (ACC) activity elicited by the cues was inversely associated with the insula and amygdala responses to aversive pictures following the cues. Nearly 75% of subjects overestimated the frequency of aversive pictures following uncertain cues, and ACC and insula activity predicted this uncertainty-related covariation bias. Findings provide the first evidence of the brain mechanisms of covariation bias and highlight the temporal dynamics of ACC, insula, and amygdala recruitment for processing aversion in the context of uncertainty.

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AIC responses to expected aversive stimuli are larger if expectations are uncertain.
“AIC responses to expected aversive stimuli are larger if expectations are uncertain”
From An Interoceptive Predictive Coding Model of Conscious Presence (2012) · cites this paper as Sarinopoulos et al., 2010
The Discussion reports larger responses to aversive pictures after uncertain than certain cues, but locates this effect in the mid-insula, not the anterior insular cortex (AIC). The Brain Activation to Aversion and Uncertainty section instead reports greater left anterior-insula activity while anticipating the certain aversive cue. Page numbers were not available in our copy. (LLM, conf=0.89)
Experimental — accuracy not yet measured
Insula and amygdala responses were larger after an uncertain cue than a certain cue.
“In their study, insula and amygdala responses were larger after an uncertain cue than a certain cue.”
From Extension of the Transdiagnostic Model to Focus on Intolerance of Uncertainty: A Review of the Literature and Implications for Treatment (2014) · cites this paper as Sarinopoulos et al. (2010)
Instructed fear studies examining anticipation of and responses to briefly presented aversive pictures revealed dorsal amygdala activation when aversive events were predictably signaled.
“Studies of instructed fear that have examined neural activity underlying both anticipation of and responses to briefly presented aversive pictures have also revealed dorsal amygdala activation (Mackiewicz et al., 2006; Nitschke et al., 2006), provided that the aversive events are predictably signaled (Sarinopoulos et al., 2010).”
From Phasic and sustained fear in humans elicits distinct patterns of brain activity (2011) · cites this paper as Sarinopoulos et al., 2010
Sources in the insula and amygdala corroborate imaging results, specifically uncertainty-related amygdalar hyperactivity in pediatric anxiety.
“Particularly, sources in the insula and amygdala, known to process subjective salience (Davis, & Whalen, 2001;Straube, & Miltner, 2011), corroborate imaging results, specifically uncertainty-related amygdalar hyperactivity in pediatric anxiety (Sarinopoulos et al., 2010;Williams et al., 2015).”
From Uncertainty increases neural indices of attention in obsessive-compulsive disorder (2017) · cites this paper as Sarinopoulos et al., 2010

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Advance Access publication August 13, 2009 Uncertainty during Anticipation Modulates Neural Responses to Aversion in Human
Sarinopoulos, I., Grupe, D. W., Mackiewicz, K. L., Herrington, D., Lor, M., Steege, E. E., & Nitschke, J. B. (2016)
Self-citation
Cerebral Cortex doi:10.1093/cercor/bhp155 Uncertainty during Anticipation Modulates Neural Responses to Aversion in Human
Sarinopoulos, I., Grupe, D. W., Mackiewicz, K. L., Herrington, D., Lor, M., Steege, E. E., & Nitschke, J. B. (2016)
Self-citation
Anticipation of Uncertain Threat Modulates Subsequent Affective Responses and Covariation Bias
Qiao, Z., Geng, H.-Y., Wang, Y., & Li, X. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.02547 · Cited by 15 · see citing works
Uncertainty is associated with biased expectancies and heightened responses to aversion.
Grupe, D. W., & Nitschke, J. B. (2011) · Emotion · doi:10.1037/a0022583 · Cited by 145 · see citing works
Self-citation
Anterior insula responds to temporally unpredictable aversiveness
Shankman, S. A., Gorka, S. M., Nelson, B. D., Fitzgerald, D. A., Phan, K. L., & O’Daly, O. (2014) · Neuroreport · doi:10.1097/wnr.0000000000000144 · Cited by 77 · see citing works

Authors: Sarinopoulos, I., Grupe, D. W., Mackiewicz, K. L., Herrington, J. D., Lor, M., Steege, E. E., & Nitschke, J. B.
Affiliations: Michigan State University (US)
University of Wisconsin–Madison (US)
University of Colorado Boulder (US)
Children's Hospital of Philadelphia (US)
Columbia University (US)
West Virginia University (US)
ORCID: Sarinopoulos, I.
Grupe, D. W.
Herrington, J. D.
Venue: Cerebral Cortex
Publisher: Oxford University Press (OUP)
Published: 2009-08-13
Volume: 20
Issue: 4
Pages: 929-940
ISSN: 1047-3211 (ISSN-L)
1460-2199
DOI: 10.1093/cercor/bhp155
PMC: PMC2837092
OpenAlex: W2138497717
Cited by: 241
References: 114
Citations by year: 2026: 5 · 2025: 10 · 2024: 9 · 2023: 9 · 2022: 18 · 2021: 15 · 2020: 11 · 2019: 9 · 2018: 22 · 2017: 14 · 2016: 18 · 2015: 18 · 2014: 21 · 2013: 20 · 2012: 17
FWCI: 6.61
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Cerebral Cortex (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Waisman Center (HD03352)
National Institutes of Health (5k02mh082130-05)
National Institute of Mental Health (K02‑MH082130, P30-HD03352, R01MH074847, K08MH063984, R01-MH74847, K08-MH63984)
National Institute of Child Health and Human Development (P30HD03352, HD03352)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD03352., P30HD003352)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
Keywords: uncertainty, anticipation, aversion, insula, amygdala, anterior cingulate cortex, anxiety, stress, aversive stimuli, expectations, temporal dynamics of neural responses
MeSH terms: Affect, Amygdala, Avoidance Learning, Brain Mapping, Cues, Female, Gyrus Cinguli, Humans, Image Processing, Computer-Assisted, Functional Laterality, Magnetic Resonance Imaging, Male, Neuropsychological Tests, Oxygen, Photic Stimulation, Uncertainty, Young Adult

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Uncertainty during anticipation modulates neural responses to aversion in human insula and amygdala

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