Cited by 176Action Observation and SynchronizationFace Recognition and PerceptionChild and Animal Learning Development

The DOI matches its Crossref record; 80 of the 81 references it cites were found in a registry or an index; none of the 43 sources its claims cite is checked for support yet.

Brain mechanisms underlying the impact of attachment-related stress on social cognition

Open access

Abstract

Mentalizing, in particular the successful attribution of complex mental states to others, is crucial for navigating social interactions. This ability is highly influenced by external factors within one's daily life, such as stress. We investigated the impact of stress on the brain basis of mentalization in adults. Using a novel modification of the Reading the Mind in the Eyes Test (RMET-R) we compared the differential effects of two personalized stress induction procedures: a general stress induction (GSI) and an attachment-related stress induction (ASI). Participants performed the RMET-R at baseline and after each of the two inductions. Baseline results replicated and extended previous findings regarding the neural correlates of the RMET-R. Additionally, we identified brain regions associated with making complex age judgments from the same stimuli. Results after stress exposure showed that the ASI condition resulted in reduced mentalization-related activation in the left posterior superior temporal sulcus (STS), left inferior frontal gyrus and left temporoparietal junction (TPJ). Moreover, the left middle frontal gyrus and left anterior insula showed greater functional connectivity to the left posterior STS after the ASI. Our findings indicate that attachment-related stress has a unique effect on the neural correlates of mentalization.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

This fMRI study compared attachment-related stress induction (ASI) with general stress induction (GSI) on mentalization using a revised Reading the Mind in the Eyes Test. ASI reduced mental-state accuracy and decreased activation in left posterior STS, left IFG, and left TPJ, with altered left posterior STS functional connectivity.

Key findings

  • At baseline, mental state > age judgments activated bilateral IFG (right t = 6.75; left t = 10.04), right posterior STS (t = 5.43), left posterior STS (t = 8.56), and dorsoMPFC (t = 6.51), among other regions; age > mental state judgments activated bilateral inferior parietal lobules, PCC/precuneus, right DLPFC, right inferior temporal gyrus, and left cerebellum.
  • Mental-state correct responses differed across conditions (F(2,24) = 3.59, p = 0.04), with lowest accuracy post-ASI (67.03%) vs baseline (74.70%) and post-GSI (74.98%); baseline vs post-ASI t(12) = 2.30, p < 0.05, and post-GSI vs post-ASI t(12) = 2.20, p < 0.05. Mental-state reaction times also differed (F(2,24) = 10.13, p = 0.01), with longest at baseline and shortest post-ASI. Age judgments showed no significant differences.
  • Post-ASI vs post-GSI during mental-state judgments showed reduced activation in left IFG (t = −2.93, p = 0.011; did not survive cluster correction), left posterior STS (t = −5.02, p < 0.001), and left TPJ (t = −4.83, p < 0.001). During age judgments, only left TPJ differed (t = −5.08, p < 0.001).
  • After ASI vs GSI, mental-state judgments showed greater functional connectivity to left posterior STS in left MFG (t = 4.90, p < 0.001) and left anterior insula (t = 5.24, p < 0.001). During age judgments, cuneus showed greater post-ASI connectivity, while bilateral anterior insula, right MTG/PHG/FFG, right dorsal ACC, and left FFG showed greater post-GSI connectivity.

Methods

  • Eighteen healthy right-handed adults were recruited; 15 remained for fMRI analysis (8 male; mean age 20.73 years, SD = 1.20, range 18–23), and behavioral analyses included 13 participants. Participants completed three fMRI runs: baseline, post-GSI, and post-ASI, with order balanced across participants. Personalized stress imagery scripts were created from recalled events rated 8 or above on a 10-point perceived stress scale.
  • The task was a revised RMET (RMET-R) with mental-state and age-judgment blocks; stimuli were shown for 3500 ms with 500 ms fixation, six trials per block, four blocks per task per condition. fMRI data were analyzed in Brain Voyager QX using random-effects GLMs; baseline mental state vs age contrast used FDR q < 0.05 with clusters ≥ 4 voxels. Stressor comparisons used a baseline-derived mask and paired t-tests (p < 0.05, cluster ≥ 4 voxels); PPI connectivity used a left posterior STS seed with cluster threshold 34 voxels.

Limitations

  • The paper states: the sample was relatively small (15 fMRI, 13 behavioral, 12 overlapping), preventing direct behavior–fMRI correlations and gender-difference analyses; the age control task’s difficulty/cognitive load was not well quantified; the sample lacked ethnic and developmental diversity; no psychophysiological indices such as heart rate variability or cortisol were reported; and the design cannot rule out other induced emotions, general social-script effects, positive-script priming, or whether effects are due to social vs non-social stressor nature or individual attachment differences.
  • The text also makes evident that the left IFG stress effect did not survive cluster correction, and behavioral data were lost for three participants due to software errors.

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Integrity signals

Registry

Crossref · 10.3389/fnhum.2013.00816

Cites

80 of 80 references verified0 citation errors · 0 not checkable

Statistics

Figures

Figure 1 Regions differentially activated by mental state and age judgments in the RMET-R administered with no previous stress induction. Regions in orange showed more activation to mental state judgments, while regions in blue showed more activation to age judgments (random-effects GLM, q < 0.05, k = 4). Data is interpolated to 1 mm3 resolution for presentation.
Figure 1 Regions differentially activated by mental state and age judgments in the RMET-R administered with no previous stress induction. Regions in orange showed more activation to mental state judgments, while regions in blue showed more activation to age judgments (random-effects GLM, q < 0.05, k = 4). Data is interpolated to 1 mm3 resolution for presentation.CC BY · PubMed Central
Figure 2 Left: Regions that showed differential activation between mental state and age judgments in the baseline RMET-R that were modulated by stress induction type during mental state judgments. Right: Regions that showed differential activation between mental state and age judgments in the baseline RMET-R that were modulated by stress induction type during age judgments. Regions in blue reflect decreased activation post-ASI compared with post-GSI (masked voxel-wise paired t-test, p < 0.05, k = 4). Data is interpolated to 1 mm3 resolution for presentation.
Figure 2 Left: Regions that showed differential activation between mental state and age judgments in the baseline RMET-R that were modulated by stress induction type during mental state judgments. Right: Regions that showed differential activation between mental state and age judgments in the baseline RMET-R that were modulated by stress induction type during age judgments. Regions in blue reflect decreased activation post-ASI compared with post-GSI (masked voxel-wise paired t-test, p < 0.05, k = 4). Data is interpolated to 1 mm3 resolution for presentation.CC BY · PubMed Central
Figure 3 Differential functional connectivity to the left posterior STS during mental state and age judgments after the ASI vs. the GSI. Regions in orange showed greater functional connectivity to the left posterior STS during judgments post-ASI. Regions in blue showed greater functional connectivity to the left posterior STS during judgments post-GSI (p < 0.05, k = 34). The seed region for the connectivity analysis (shown in purple) was defined by greater activation to mental state judgments compared with age judgments in the RMET-R at baseline. Data is interpolated to 1 mm3 resolution for presentation.
Figure 3 Differential functional connectivity to the left posterior STS during mental state and age judgments after the ASI vs. the GSI. Regions in orange showed greater functional connectivity to the left posterior STS during judgments post-ASI. Regions in blue showed greater functional connectivity to the left posterior STS during judgments post-GSI (p < 0.05, k = 34). The seed region for the connectivity analysis (shown in purple) was defined by greater activation to mental state judgments compared with age judgments in the RMET-R at baseline. Data is interpolated to 1 mm3 resolution for presentation.CC BY · PubMed Central
Figure A1 Examples of single trials. (A) emotion recognition task; (B) control task, age judgments.
Figure A1 Examples of single trials. (A) emotion recognition task; (B) control task, age judgments.CC BY · PubMed Central

Verification

Claims the paper makes

23 Own result · 22 Not checked yet · 17 Own method · 11 Own interpretation · 3 No basis given

Verify all 43 references — free account
  • Probably not a substantial claim. 18
  • It may state two separate claims as one. 18
  • The quote only partly states this claim. 1
31 of 31
  • The paper relies on this without support.

    The personalized ASI and GSI scripts successfully induced the intended attachment-related and general stress states, respectively.

    “In this way, two types of inductions were created: attachment-related stress inductions (ASI) and general stress inductions (GSI).”
  • The paper relies on this without support.

    The modified age-judgment task is a valid control for mental state judgments, isolating mentalization-related processes.

    “This modification was implemented in order to increase the difficulty of the control task, rendering it more comparable to the experimental task.”
  • The paper relies on this without support.

    The attachment-related and general stress inductions induced comparable levels of general stress, so differences between them can be attributed to attachment-related content rather than stress intensity.

    “While we took efforts to match the inductions on the level of induced stress, we do not have data that speak to the simultaneous induction of other emotions and underpinning neural networks that may have occurred with more intensity during ASI (such as fear, anger, sadness, or a complex combination thereof).”
  • The paper relies on this without support.

    The age judgment task and the mental state judgment task are comparable in difficulty or cognitive load, so differential activation can be interpreted as task-specific.

    “limitations related to the age task should be addressed in future studies by using a task for which the difficulty or cognitive load between task and control task can be quantified better.”
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Statistics recomputed

Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.

  • Consistentt(14) = 1.07reported p = .34 · recomputed p = .303

    “t(14) = 1.07, p = .34”

    The paper states a false-discovery-rate adjustment

  • Consistentt(12) = 0.21reported p = .84 · recomputed p = .837

    “t(12) = 0.21, p = .84”

  • Consistentt(12) = 1.89reported p = .08 · recomputed p = .083

    “t(12) = 1.89, p = .08”

  • Consistentt(12) = 2.3reported p < .05 · recomputed p = .040

    “t(12) = 2.30, p < .05”

  • Consistentt(12) = 2.2reported p < .05 · recomputed p = .048

    “t(12) = 2.20, p < .05”

  • Consistentt(12) = 4.12reported p < .01 · recomputed p = .001

    “t(12) = 4.12, p < .01”

  • Consistentt(12) = 3.65reported p < .01 · recomputed p = .003

    “t(12) = 3.65, p < .01”

  • ConsistentF(2, 24) = 10.13reported p = .01 · recomputed p < .001

    “F(2, 24) = 10.13, p = .01”

    The paper prints p at a floor (such as p < .001)

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Metadata

Authors
Nolte, T., Bolling, D. Z., Hudac, C. M., Fonagy, P., Mayes, L., & Pelphrey, K. A.
Affiliations
  • Wellcome Centre for Human Neuroimaging (GB)
  • Yale University (US)
  • University of Nebraska–Lincoln (US)
Corresponding author
Nolte, Tobias
Venue
Frontiers in Human Neuroscience
Published
2013
Volume
7
Pages
816-816
ISSN
1662-5161 (ISSN-L)
OpenAlex
W2104967339
Cited by
176
References
81
Citations by year
2026: 8 · 2025: 18 · 2024: 18 · 2023: 20 · 2022: 10 · 2021: 20 · 2020: 16 · 2019: 12 · 2018: 9 · 2017: 9 · 2016: 22 · 2015: 9 · 2014: 2 · 2013: 1
FWCI
16.96
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Human Neuroscience (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Lincoln (University of Nebraska) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • UCL Discovery (University College London) (submittedVersion)
Funders
  • International Psychoanalytical Association
  • National Institute for Health and Care Research (NF-SI-0510-10228)
  • National Institute of Mental Health (R01MH084080)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD057173)
Topics
  • Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
  • Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
Keywords
mentalization, social cognition, theory of mind, stress induction, Reading the Mind in the Eyes Test, posterior superior temporal sulcus, temporoparietal junction, inferior frontal gyrus, anterior insula, middle frontal gyrus, functional connectivity

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