The Double-edged Sword of the Hippocampus-ventromedial Prefrontal Cortex Resting-state Connectivity in Stress Susceptibility and Resilience: A Prospective Study

Overview

Journal Neurobiol Stress

Date 2023 Nov 15

PMID 37965440

Authors

Jingjing Chang

Di Song

Rongjun Yu

Affiliations

Soon will be listed here.

Abstract

The hippocampus has long been considered a pivotal region implicated in both stress susceptibility and resilience. A wealth of evidence from animal and human studies underscores the significance of hippocampal functional connectivity with the ventromedial prefrontal cortex (vmPFC) in these stress-related processes. However, there remains a scarcity of research that explores and contrasts the roles of hippocampus-vmPFC connectivity in stress susceptibility and resilience when facing a real-life traumatic event from a prospective standpoint. In the present study, we investigated the contributions of undirected and directed connectivity between the hippocampus and vmPFC to stress susceptibility and resilience within the context of the COVID-19 pandemic. Our findings revealed that the left hippocampus-left vmPFC connectivity prior to the pandemic exhibited a negative correlation with both stress susceptibility and resilience. Specifically, individuals with stronger left hippocampus-left vmPFC connectivity reported experiencing fewer stress-related feelings during the outbreak period of the epidemic but displayed lower levels of stress resilience five months later. Our application of spectral dynamic causal modeling unveiled an additional inhibitory connectivity pathway from the left hippocampus to the left vmPFC in the context of stress susceptibility, which was notably absent in stress resilience. Furthermore, we observed a noteworthy positive association between self-inhibition of the vmPFC and stress susceptibility, with this effect proving substantial enough to predict an individual's susceptibility to stress; conversely, these patterns did not manifest in the realm of stress resilience. These findings enrich our comprehension of stress susceptibility and stress resilience and might have implications for innovative approaches to managing stress-related disorders.

Citing Articles

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References

Morey R, Haswell C, Hooper S, De Bellis M . Amygdala, Hippocampus, and Ventral Medial Prefrontal Cortex Volumes Differ in Maltreated Youth with and without Chronic Posttraumatic Stress Disorder. Neuropsychopharmacology. 2015; 41(3):791-801. PMC: 4707825. DOI: 10.1038/npp.2015.205. View

Watson P . Stress, PTSD, and COVID-19: the Utility of Disaster Mental Health Interventions During the COVID-19 Pandemic. Curr Treat Options Psychiatry. 2022; 9(1):14-40. PMC: 8860255. DOI: 10.1007/s40501-021-00253-z. View

Nathan Spreng R, Mar R, Kim A . The common neural basis of autobiographical memory, prospection, navigation, theory of mind, and the default mode: a quantitative meta-analysis. J Cogn Neurosci. 2008; 21(3):489-510. DOI: 10.1162/jocn.2008.21029. View

Nelson M, Tumpap A . Posttraumatic stress disorder symptom severity is associated with left hippocampal volume reduction: a meta-analytic study. CNS Spectr. 2016; 22(4):363-372. DOI: 10.1017/S1092852916000833. View

Motzkin J, Philippi C, Wolf R, Baskaya M, Koenigs M . Ventromedial prefrontal cortex is critical for the regulation of amygdala activity in humans. Biol Psychiatry. 2014; 77(3):276-284. PMC: 4145052. DOI: 10.1016/j.biopsych.2014.02.014. View

Friston K, Kahan J, Biswal B, Razi A . A DCM for resting state fMRI. Neuroimage. 2013; 94:396-407. PMC: 4073651. DOI: 10.1016/j.neuroimage.2013.12.009. View

Larosa A, Wong T . The hippocampus in stress susceptibility and resilience: Reviewing molecular and functional markers. Prog Neuropsychopharmacol Biol Psychiatry. 2022; 119:110601. DOI: 10.1016/j.pnpbp.2022.110601. View

Postel C, Mary A, Dayan J, Fraisse F, Vallee T, Guillery-Girard B . Variations in response to trauma and hippocampal subfield changes. Neurobiol Stress. 2021; 15:100346. PMC: 8170416. DOI: 10.1016/j.ynstr.2021.100346. View

Zeev-Wolf M, Levy J, Goldstein A, Zagoory-Sharon O, Feldman R . Chronic Early Stress Impairs Default Mode Network Connectivity in Preadolescents and Their Mothers. Biol Psychiatry Cogn Neurosci Neuroimaging. 2018; 4(1):72-80. DOI: 10.1016/j.bpsc.2018.09.009. View

10.

Admon R, Milad M, Hendler T . A causal model of post-traumatic stress disorder: disentangling predisposed from acquired neural abnormalities. Trends Cogn Sci. 2013; 17(7):337-47. DOI: 10.1016/j.tics.2013.05.005. View

11.

Razi A, Kahan J, Rees G, Friston K . Construct validation of a DCM for resting state fMRI. Neuroimage. 2014; 106:1-14. PMC: 4295921. DOI: 10.1016/j.neuroimage.2014.11.027. View

12.

Hamilton J, Furman D, Chang C, Thomason M, Dennis E, Gotlib I . Default-mode and task-positive network activity in major depressive disorder: implications for adaptive and maladaptive rumination. Biol Psychiatry. 2011; 70(4):327-33. PMC: 3144981. DOI: 10.1016/j.biopsych.2011.02.003. View

13.

Lanius R, Frewen P, Tursich M, Jetly R, McKinnon M . Restoring large-scale brain networks in PTSD and related disorders: a proposal for neuroscientifically-informed treatment interventions. Eur J Psychotraumatol. 2015; 6:27313. PMC: 4390556. DOI: 10.3402/ejpt.v6.27313. View

14.

Chang J, Yu R . Acute social stress modulates coherence regional homogeneity. Brain Imaging Behav. 2018; 13(3):762-770. DOI: 10.1007/s11682-018-9898-9. View

15.

Nitschke J, Forbes P, Ali N, Cutler J, Apps M, Lockwood P . Resilience during uncertainty? Greater social connectedness during COVID-19 lockdown is associated with reduced distress and fatigue. Br J Health Psychol. 2020; 26(2):553-569. PMC: 8247344. DOI: 10.1111/bjhp.12485. View

16.

Pruessner J, Baldwin M, Dedovic K, Renwick R, Mahani N, Lord C . Self-esteem, locus of control, hippocampal volume, and cortisol regulation in young and old adulthood. Neuroimage. 2005; 28(4):815-26. DOI: 10.1016/j.neuroimage.2005.06.014. View

17.

Pitman R, Gilbertson M, Gurvits T, May F, Lasko N, Metzger L . Clarifying the origin of biological abnormalities in PTSD through the study of identical twins discordant for combat exposure. Ann N Y Acad Sci. 2006; 1071:242-54. PMC: 2770249. DOI: 10.1196/annals.1364.019. View

18.

Johnstone T, van Reekum C, Urry H, Kalin N, Davidson R . Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J Neurosci. 2007; 27(33):8877-84. PMC: 6672169. DOI: 10.1523/JNEUROSCI.2063-07.2007. View

19.

Wu J, Szpunar K, Godovich S, Schacter D, Hofmann S . Episodic future thinking in generalized anxiety disorder. J Anxiety Disord. 2015; 36:1-8. PMC: 4658269. DOI: 10.1016/j.janxdis.2015.09.005. View

20.

Uy J, Galvan A . Acute stress increases risky decisions and dampens prefrontal activation among adolescent boys. Neuroimage. 2016; 146:679-689. DOI: 10.1016/j.neuroimage.2016.08.067. View