Probing the neurocardiac circuit in trauma and posttraumatic stress - PubMed (original) (raw)

doi: 10.1016/j.jpsychires.2024.06.009. Epub 2024 Jun 7.

Nathaniel G Harnett 2, Robyn A Ellis 2, Lana R Grasser 3, Mubeena Hanif 3, Charis Wiltshire 3, Timothy D Ely 4, Lauren A M Lebois 2, Sanne J H van Rooij 4, Stacey L House 5, Francesca L Beaudoin 6, Xinming An 7, Thomas C Neylan 8, Gari D Clifford 9, Sarah D Linnstaedt 7, Laura T Germine 10, Kenneth A Bollen 11, Scott L Rauch 12, John P Haran 13, Alan B Storrow 14, Christopher Lewandowski 15, Paul I Musey Jr 16, Phyllis L Hendry 17, Sophia Sheikh 17, Christopher W Jones 18, Brittany E Punches 19, Robert A Swor 20, Lauren A Hudak 21, Jose L Pascual 22, Mark J Seamon 23, Erica Harris 24, Claire Pearson 25, David A Peak 26, Roland C Merchant 27, Robert M Domeier 28, Niels K Rathlev 29, Brian J O'Neil 30, Paulina Sergot 31, Leon D Sanchez 32, Steven E Bruce 33, Steven E Harte 34, Karestan C Koenen 35, Ronald C Kessler 36, Samuel A McLean 37, Kerry J Ressler 2, Jennifer S Stevens 4, Tanja Jovanovic 3

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Probing the neurocardiac circuit in trauma and posttraumatic stress

Antonia V Seligowski et al. J Psychiatr Res. 2024 Aug.

Abstract

The neurocardiac circuit is integral to physiological regulation of threat and trauma-related responses. However, few direct investigations of brain-behavior associations with replicable physiological markers of PTSD have been conducted. The current study probed the neurocardiac circuit by examining associations among its core regions in the brain (e.g., insula, hypothalamus) and the periphery (heart rate [HR], high frequency heart rate variability [HF-HRV], and blood pressure [BP]). We sought to characterize these associations and to determine whether there were differences by PTSD status. Participants were N = 315 (64.1 % female) trauma-exposed adults enrolled from emergency departments as part of the prospective AURORA study. Participants completed a deep phenotyping session (e.g., fear conditioning, magnetic resonance imaging) two weeks after emergency department admission. Voxelwise analyses revealed several significant interactions between PTSD severity 8-weeks posttrauma and psychophysiological recordings on hypothalamic connectivity to the prefrontal cortex (PFC), insula, superior temporal sulcus, and temporoparietaloccipital junction. Among those with PTSD, diastolic BP was directly correlated with right insula-hypothalamic connectivity, whereas the reverse was found for those without PTSD. PTSD status moderated the association between systolic BP, HR, and HF-HRV and hypothalamic connectivity in the same direction. While preliminary, our findings may suggest that individuals with higher PTSD severity exhibit compensatory neural mechanisms to down-regulate autonomic imbalance. Additional study is warranted to determine how underlying mechanisms (e.g., inflammation) may disrupt the neurocardiac circuit and increase cardiometabolic disease risk in PTSD.

Keywords: Autonomic; Cardiovascular; Connectivity; Imaging; PTSD; Trauma.

Copyright © 2024 Elsevier Ltd. All rights reserved.

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Conflict of interest statement

Declaration of competing interest Dr. Neylan reports consultation for Jazz Pharmaceuticals; Dr. Rauch reports royalties from Oxford University Press, the American Psychiatric Publishing Inc., and Springer Publishing royalties; Dr. McLean reports consultation for Walter Reed Army Institute for Research and for Arbor Medical Innovations; Dr. Kessler reports consultation for Cambridge Health Alliance, Canandaigua VA Medical Center, Holmusk, Partners Healthcare, INC Mirah, PYM, and Roga Sciences; Dr. Koenen reports royalties from Guilford Press and Oxford University Press; Dr. Ressler reports consultation for Bioxcel, Bionomics, Acer, and Jazz Pharma; All other authors report no biomedical financial interests or potential conflicts of interest.

Figures

Figure 1.

Figure 1.. PTSD moderates the association between diastolic BP and hypothalamic connectivity.

Note. A) PTSD status significantly moderated the association between diastolic BP and hypothalamus connectivity to several brain regions including the insula (dark blue). B) Simple slopes analyses revealed participants with PTSD (cyan) showed a positive association between Diastolic BP and connectivity whereas participants without PTSD (red) showed an inverse relationship. BP = blood pressure.

Figure 2.

Figure 2.. PTSD moderates the association between systolic BP and hypothalamic connectivity.

Note. A) PTSD status significantly moderated the association between diastolic BP and hypothalamus connectivity to several brain regions including the MTG (green). B) Simple slopes analyses revealed participants with PTSD (cyan) showed a positive association between Systolic BP and connectivity whereas participants without PTSD (red) showed an orthogonal relationship. BP = blood pressure; MTG = middle temporal gyrus.

Figure 3.

Figure 3.. PTSD moderates the association between HR and hypothalamic connectivity.

Note. A) PTSD status significantly moderated the association between HR during acquisition (red) and extinction (blue) of conditioned fear and hypothalamus connectivity to the PFC (overlap shown in purple). B) Simple slopes analyses revealed participants with PTSD (cyan) showed a positive association between HR (acquisition and extinction) and connectivity whereas participants without PTSD (red) showed an inverse relationship. HR = heart rate; PFC = prefrontal cortex.

Figure 4.

Figure 4.. PTSD moderates the association between HRV and hypothalamic connectivity.

Note. A) PTSD status significantly moderated the association between HRV during extinction of conditioned fear and hypothalamus connectivity to the STS (dark blue). B) Simple slopes analyses revealed participants with PTSD (cyan) showed a negative association between HRV and connectivity whereas participants without PTSD (red) showed an orthogonal relationship. HRV = heart rate variability; STS = superior temporal sulcus.

References

    1. Belleau EL, Ehret LE, Hanson JL, Brasel KJ, Larson CL, deRoon-Cassini TA, 2020. Amygdala functional connectivity in the acute aftermath of trauma prospectively predicts severity of posttraumatic stress symptoms. Neurobiology of Stress 12, 100217. 10.1016/j.ynstr.2020.100217 -DOI -PMC -PubMed
    1. Ben-Zion Z, Artzi M, Niry D, Keynan NJ, Zeevi Y, Admon R, Sharon H, Halpern P, Liberzon I, Shalev AY, Hendler T, 2020. Neuroanatomical Risk Factors for Posttraumatic Stress Disorder in Recent Trauma Survivors. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging 5, 311–319. 10.1016/j.bpsc.2019.11.003 -DOI -PMC -PubMed
    1. Berntson GG, Thomas Bigger J, Eckberg DL, Grossman P, Kaufmann PG, Malik M, Nagaraja HN, Porges SW, Saul JP, Stone PH, Van Der Molen MW, 1997. Heart rate variability: Origins, methods, and interpretive caveats. Psychophysiology 34, 623–648. 10.1111/j.1469-8986.1997.tb02140.x -DOI -PubMed
    1. Blechert J, Michael T, Grossman P, Lajtman M, Wilhelm FH, 2007. Autonomic and Respiratory Characteristics of Posttraumatic Stress Disorder and Panic Disorder. Psychosomatic Medicine 69, 935–943. 10.1097/PSY.0b013e31815a8f6b -DOI -PubMed
    1. Bourassa KJ, Stevens ES, Katz AC, Rothbaum BO, Reger GM, Norr AM, 2020. The Impact of Exposure Therapy on Resting Heart Rate and Heart Rate Reactivity Among Active-Duty Soldiers With Posttraumatic Stress Disorder. Psychosomatic Medicine 82, 108. 10.1097/PSY.0000000000000758 -DOI -PubMed

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