Cortical and subcortical mapping of the allostatic-interoceptive system in the human brain: replication and extension with 7 Tesla fMRI

Zhang, Jiahe; Chen, Danlei; Srirangarajan, Tara; Theriault, Jordan; Kragel, Philip A.; Hartley, Ludger; Lee, Kent M.; McVeigh, Kieran; Wager, Tor D.; Wald, Lawrence L.; Satpute, Ajay B.; Quigley, Karen S.; Whitfield-Gabrieli, Susan; Barrett, Lisa Feldman; Bianciardi, Marta

doi:10.1101/2023.07.20.548178

Cited by 3 publications

(1 citation statement)

References 139 publications

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“…These areas are part of what has been termed a ‘visceral control network’, which is proposed to be involved in mediating psychological stress appraisals and simultaneously controlling cardiovascular physiology, with alterations in this network being linked to a higher risk of cardiovascular disease 9 . These brain systems have also been recently described as belonging to an interoceptive-allostatic brain network for regulating peripheral physiology by predictive or anticipatory processes 66,67 . Along similar lines, our results appear to provide evidence for a pathway whereby increased brain activity in systems encompassed by these networks associates with larger rises in stressor-evoked systolic blood pressure and preclinical atherosclerosis across people.…”

Section: Discussionmentioning

confidence: 99%

Stressor-evoked brain activity, cardiovascular reactivity, and subclinical atherosclerosis in midlife adults

Rasero,

Verstynen,

DuPont

et al. 2024

Preprint

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BackgroundCardiovascular responses to psychological stressors have been separately associated with preclinical atherosclerosis and hemodynamic brain activity patterns across different studies and cohorts; however, what has not been established is whether cardiovascular stress responses reliably link indicators of stressor-evoked brain activity and preclinical atherosclerosis that have been measured in the same individuals. Accordingly, the present study used cross-validation and predictive modeling to test for the first time whether stressor-evoked systolic blood pressure (SBP) responses statistically mediated the association between concurrently measured brain activity and a vascular marker of preclinical atherosclerosis in the carotid arteries.Methods624 midlife adults (aged 28-56 years, 54.97% female) from two different cohorts underwent two information-conflict fMRI tasks, with concurrent SBP measures collected. Carotid artery intima-media thickness (CA-IMT) was measured by ultrasonography. A mediation framework that included harmonization, cross-validation, and penalized principal component regression was then employed, while significant areas in possible direct and indirect effects were identified through bootstrapping. Sensitivity analysis further tested the robustness of findings after accounting for prevailing levels of cardiovascular disease risk and brain imaging data quality control.ResultsTask-averaged patterns of hemodynamic brain responses exhibited a generalizable association with CA-IMT, which was mediated by an area-under-the-curve measure of aggregate SBP reactivity. Importantly, this effect held in sensitivity analyses. Implicated brain areas in this mediation included the ventromedial prefrontal cortex, anterior cingulate cortex, insula and amygdala.ConclusionsThese novel findings support a link between stressor-evoked brain activity and preclinical atherosclerosis accounted for by individual differences in corresponding levels of stressor-evoked cardiovascular reactivity.

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Section: Discussionmentioning

confidence: 99%

Stressor-evoked brain activity, cardiovascular reactivity, and subclinical atherosclerosis in midlife adults

Rasero,

Verstynen,

DuPont

et al. 2024

Preprint

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The association between early regulatory problems and adult peer relationship quality is mediated by the brain's allostatic‐interoceptive system

Zorjan,

Wolke,

Baumann

et al. 2024

Child Psychology Psychiatry

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BackgroundEarly regulatory problems (RPs), i.e., problems with crying, sleeping, and/or feeding during the first years, increase the risk for avoidant personality traits in adulthood, associated with social withdrawal and anxiety. Even more, RPs are linked with functional alterations in the adult default mode and salience networks, comprising the brain's allostatic‐interoceptive system (AIS) and playing a role in social interactions. We investigated whether RPs assessed in infancy are associated with difficulties in adult peer relationships mediated by functional alterations of the AIS.MethodsAs part of a large case‐controlled prospective study, 42 adults with previous RPs and 70 matched controls (mean age = 28.48, SD = 2.65, 51% male) underwent fMRI during rest. The analysis focused on the intrinsic functional connectivity (iFC) of key nodes of the AIS. Peer relationship quality was assessed via a semi‐structured Life Course Interview and the YASR scale. In these same individuals, RPs were assessed at ages 5, 20 and 56 months.ResultsRPs in infancy were associated with lower‐quality peer relationships and enhanced functional connectivity of the AIS nodes in adulthood, with a stronger effect for multiple and persistent RPs compared with transient‐multiple or single‐persistent RPs. Importantly, iFC changes of the dorsal mid insula, a primary interoceptive cortex with frontal and temporal regions, mediated the relationship between early RPs and adult peer relationship quality.ConclusionsResults indicate long‐lasting social and neural changes associated with early RPs. Our findings further implicate the AIS in both interoceptive and social processes, while indicating the need for early screening of early RPs.

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Cortical and subcortical brain networks predict prevailing heart rate

Sentis,

Rasero,

Gianaros

et al. 2024

Psychophysiology

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Resting heart rate may confer risk for cardiovascular disease (CVD) and other adverse cardiovascular events. While the brainstem's autonomic control over heart rate is well established, less is known about the regulatory role of higher level cortical and subcortical brain regions, especially in humans. This study sought to characterize the brain networks that predict variation in prevailing heart rate in otherwise healthy adults. We used machine learning approaches designed for complex, high‐dimensional data sets, to predict variation in instantaneous heart period (the inter‐heartbeat‐interval) from whole‐brain hemodynamic signals measured by fMRI. Task‐based and resting‐state fMRI, as well as peripheral physiological recordings, were taken from two data sets that included extensive repeated measurements within individuals. Our models reliably predicted instantaneous heart period from whole‐brain fMRI data both within and across individuals, with prediction accuracies being highest when measured within‐participants. We found that a network of cortical and subcortical brain regions, many linked to visceral motor and visceral sensory processes, were reliable predictors of variation in heart period. This adds to evidence on brain–heart interactions and constitutes an incremental step toward developing clinically applicable biomarkers of brain contributions to CVD risk.

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Cortical and subcortical mapping of the allostatic-interoceptive system in the human brain: replication and extension with 7 Tesla fMRI

Cited by 3 publications

References 139 publications

Stressor-evoked brain activity, cardiovascular reactivity, and subclinical atherosclerosis in midlife adults

Stressor-evoked brain activity, cardiovascular reactivity, and subclinical atherosclerosis in midlife adults

The association between early regulatory problems and adult peer relationship quality is mediated by the brain's allostatic‐interoceptive system

Cortical and subcortical brain networks predict prevailing heart rate

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