Hippocampal Threat Reactivity Interacts with Physiological Arousal to Predict PTSD Symptoms

Büşra Tanriverdi; David F. Gregory; Thomas M. Olino; Timothy D. Ely; Nathaniel G. Harnett; Sanne J.H. van Rooij; Lauren A.M. Lebois; Antonia V. Seligowski; Tanja Jovanovic; Kerry J. Ressler; Stacey L. House; Francesca L. Beaudoin; Xinming An; Thomas C. Neylan; Gari D. Clifford; Sarah D. Linnstaedt; Laura T. Germine; Kenneth A. Bollen; Scott L. Rauch; John P. Haran; Alan B. Storrow; Christopher Lewandowski; Paul I. Musey; Phyllis L. Hendry; Sophia Sheikh; Christopher W. Jones; Brittany E. Punches; Michael C. Kurz; Meghan E. McGrath; Lauren A. Hudak; Jose L. Pascual; Mark J. Seamon; Elizabeth M. Datner; Claire Pearson; Robert M. Domeier; Niels K. Rathlev; Brian J. O'Neil; Leon D. Sanchez; Steven E. Bruce; Mark W. Miller; Robert H. Pietrzak; Jutta Joormann; Deanna M. Barch; Diego A. Pizzagalli; John F. Sheridan; Jordan W. Smoller; Steven E. Harte; James M. Elliott; Samuel A. McLean; Ronald C. Kessler; Karestan C. Koenen; Jennifer S. Stevens; Vishnu P. Murty

doi:10.1523/JNEUROSCI.0838-22.2022

Hippocampal Threat Reactivity Interacts with Physiological Arousal to Predict PTSD Symptoms

Büşra Tanriverdi, David F. Gregory, Thomas M. Olino, Timothy D. Ely, Nathaniel G. Harnett, Sanne J.H. van Rooij, Lauren A.M. Lebois, Antonia V. Seligowski, Tanja Jovanovic, Kerry J. Ressler, Stacey L. House, Francesca L. Beaudoin, Xinming An, Thomas C. Neylan, Gari D. Clifford, Sarah D. Linnstaedt, Laura T. Germine, Kenneth A. Bollen, Scott L. Rauch, John P. HaranAlan B. Storrow, Christopher Lewandowski, Paul I. Musey, Phyllis L. Hendry, Sophia Sheikh, Christopher W. Jones, Brittany E. Punches, Michael C. Kurz, Meghan E. McGrath, Lauren A. Hudak, Jose L. Pascual, Mark J. Seamon, Elizabeth M. Datner, Claire Pearson, Robert M. Domeier, Niels K. Rathlev, Brian J. O'Neil, Leon D. Sanchez, Steven E. Bruce, Mark W. Miller, Robert H. Pietrzak, Jutta Joormann, Deanna M. Barch, Diego A. Pizzagalli, John F. Sheridan, Jordan W. Smoller, Steven E. Harte, James M. Elliott, Samuel A. McLean, Ronald C. Kessler, Karestan C. Koenen, Jennifer S. Stevens, Vishnu P. Murty

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8 Scopus citations

Abstract

Hippo campal impairments are reliably associated with post-traumatic stress disorder (PTSD); however, little research has characterized how increased threat sensitivity may interact with arousal responses to alter hippocampal reactivity, and further how these interactions relate to the sequelae of trauma-related symptoms. In a sample of individuals recently exposed to trauma (N = 116, 76 female), we found that PTSD symptoms at 2 weeks were associated with decreased hippocampal responses to threat as assessed with fMRI. Further, the relationship between hippocampal threat sensitivity and PTSD symptomology only emerged in individuals who showed transient, high threat-related arousal, as assayed by an independently collected measure of fear potentiated startle. Collectively, our finding suggests that development of PTSD is associated with threat-related decreases in hippocampal function because of increases in fear-potentiated arousal.

Original language	English
Pages (from-to)	6593-6604
Number of pages	12
Journal	Journal of Neuroscience
Volume	42
Issue number	34
DOIs	https://doi.org/10.1523/JNEUROSCI.0838-22.2022
State	Published - Aug 24 2022

Keywords

arousal
fMRI
fear
hippocampus
trauma

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10.1523/JNEUROSCI.0838-22.2022

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Tanriverdi, B., Gregory, D. F., Olino, T. M., Ely, T. D., Harnett, N. G., van Rooij, S. J. H., Lebois, L. A. M., Seligowski, A. V., Jovanovic, T., Ressler, K. J., House, S. L., Beaudoin, F. L., An, X., Neylan, T. C., Clifford, G. D., Linnstaedt, S. D., Germine, L. T., Bollen, K. A., Rauch, S. L., ... Murty, V. P. (2022). Hippocampal Threat Reactivity Interacts with Physiological Arousal to Predict PTSD Symptoms. Journal of Neuroscience, 42(34), 6593-6604. https://doi.org/10.1523/JNEUROSCI.0838-22.2022

@article{b231d2ad626f4af0861da394ddd1e5ef,

title = "Hippocampal Threat Reactivity Interacts with Physiological Arousal to Predict PTSD Symptoms",

abstract = "Hippo campal impairments are reliably associated with post-traumatic stress disorder (PTSD); however, little research has characterized how increased threat sensitivity may interact with arousal responses to alter hippocampal reactivity, and further how these interactions relate to the sequelae of trauma-related symptoms. In a sample of individuals recently exposed to trauma (N = 116, 76 female), we found that PTSD symptoms at 2 weeks were associated with decreased hippocampal responses to threat as assessed with fMRI. Further, the relationship between hippocampal threat sensitivity and PTSD symptomology only emerged in individuals who showed transient, high threat-related arousal, as assayed by an independently collected measure of fear potentiated startle. Collectively, our finding suggests that development of PTSD is associated with threat-related decreases in hippocampal function because of increases in fear-potentiated arousal.",

keywords = "arousal, fMRI, fear, hippocampus, trauma",

author = "B{\"u}{\c s}ra Tanriverdi and Gregory, {David F.} and Olino, {Thomas M.} and Ely, {Timothy D.} and Harnett, {Nathaniel G.} and {van Rooij}, {Sanne J.H.} and Lebois, {Lauren A.M.} and Seligowski, {Antonia V.} and Tanja Jovanovic and Ressler, {Kerry J.} and House, {Stacey L.} and Beaudoin, {Francesca L.} and Xinming An and Neylan, {Thomas C.} and Clifford, {Gari D.} and Linnstaedt, {Sarah D.} and Germine, {Laura T.} and Bollen, {Kenneth A.} and Rauch, {Scott L.} and Haran, {John P.} and Storrow, {Alan B.} and Christopher Lewandowski and Musey, {Paul I.} and Hendry, {Phyllis L.} and Sophia Sheikh and Jones, {Christopher W.} and Punches, {Brittany E.} and Kurz, {Michael C.} and McGrath, {Meghan E.} and Hudak, {Lauren A.} and Pascual, {Jose L.} and Seamon, {Mark J.} and Datner, {Elizabeth M.} and Claire Pearson and Domeier, {Robert M.} and Rathlev, {Niels K.} and O'Neil, {Brian J.} and Sanchez, {Leon D.} and Bruce, {Steven E.} and Miller, {Mark W.} and Pietrzak, {Robert H.} and Jutta Joormann and Barch, {Deanna M.} and Pizzagalli, {Diego A.} and Sheridan, {John F.} and Smoller, {Jordan W.} and Harte, {Steven E.} and Elliott, {James M.} and McLean, {Samuel A.} and Kessler, {Ronald C.} and Koenen, {Karestan C.} and Stevens, {Jennifer S.} and Murty, {Vishnu P.}",

note = "Publisher Copyright: Copyright {\textcopyright} 2022 the authors.",

year = "2022",

month = aug,

day = "24",

doi = "10.1523/JNEUROSCI.0838-22.2022",

language = "English",

volume = "42",

pages = "6593--6604",

journal = "Journal of Neuroscience",

issn = "0270-6474",

number = "34",

}

Tanriverdi, B, Gregory, DF, Olino, TM, Ely, TD, Harnett, NG, van Rooij, SJH, Lebois, LAM, Seligowski, AV, Jovanovic, T, Ressler, KJ, House, SL, Beaudoin, FL, An, X, Neylan, TC, Clifford, GD, Linnstaedt, SD, Germine, LT, Bollen, KA, Rauch, SL, Haran, JP, Storrow, AB, Lewandowski, C, Musey, PI, Hendry, PL, Sheikh, S, Jones, CW, Punches, BE, Kurz, MC, McGrath, ME, Hudak, LA, Pascual, JL, Seamon, MJ, Datner, EM, Pearson, C, Domeier, RM, Rathlev, NK, O'Neil, BJ, Sanchez, LD, Bruce, SE, Miller, MW, Pietrzak, RH, Joormann, J, Barch, DM, Pizzagalli, DA, Sheridan, JF, Smoller, JW, Harte, SE, Elliott, JM, McLean, SA, Kessler, RC, Koenen, KC, Stevens, JS & Murty, VP 2022, 'Hippocampal Threat Reactivity Interacts with Physiological Arousal to Predict PTSD Symptoms', Journal of Neuroscience, vol. 42, no. 34, pp. 6593-6604. https://doi.org/10.1523/JNEUROSCI.0838-22.2022

TY - JOUR

T1 - Hippocampal Threat Reactivity Interacts with Physiological Arousal to Predict PTSD Symptoms

AU - Tanriverdi, Büşra

AU - Gregory, David F.

AU - Olino, Thomas M.

AU - Ely, Timothy D.

AU - Harnett, Nathaniel G.

AU - van Rooij, Sanne J.H.

AU - Lebois, Lauren A.M.

AU - Seligowski, Antonia V.

AU - Jovanovic, Tanja

AU - Ressler, Kerry J.

AU - House, Stacey L.

AU - Beaudoin, Francesca L.

AU - An, Xinming

AU - Neylan, Thomas C.

AU - Clifford, Gari D.

AU - Linnstaedt, Sarah D.

AU - Germine, Laura T.

AU - Bollen, Kenneth A.

AU - Rauch, Scott L.

AU - Haran, John P.

AU - Storrow, Alan B.

AU - Lewandowski, Christopher

AU - Musey, Paul I.

AU - Hendry, Phyllis L.

AU - Sheikh, Sophia

AU - Jones, Christopher W.

AU - Punches, Brittany E.

AU - Kurz, Michael C.

AU - McGrath, Meghan E.

AU - Hudak, Lauren A.

AU - Pascual, Jose L.

AU - Seamon, Mark J.

AU - Datner, Elizabeth M.

AU - Pearson, Claire

AU - Domeier, Robert M.

AU - Rathlev, Niels K.

AU - O'Neil, Brian J.

AU - Sanchez, Leon D.

AU - Bruce, Steven E.

AU - Miller, Mark W.

AU - Pietrzak, Robert H.

AU - Joormann, Jutta

AU - Barch, Deanna M.

AU - Pizzagalli, Diego A.

AU - Sheridan, John F.

AU - Smoller, Jordan W.

AU - Harte, Steven E.

AU - Elliott, James M.

AU - McLean, Samuel A.

AU - Kessler, Ronald C.

AU - Koenen, Karestan C.

AU - Stevens, Jennifer S.

AU - Murty, Vishnu P.

PY - 2022/8/24

Y1 - 2022/8/24

N2 - Hippo campal impairments are reliably associated with post-traumatic stress disorder (PTSD); however, little research has characterized how increased threat sensitivity may interact with arousal responses to alter hippocampal reactivity, and further how these interactions relate to the sequelae of trauma-related symptoms. In a sample of individuals recently exposed to trauma (N = 116, 76 female), we found that PTSD symptoms at 2 weeks were associated with decreased hippocampal responses to threat as assessed with fMRI. Further, the relationship between hippocampal threat sensitivity and PTSD symptomology only emerged in individuals who showed transient, high threat-related arousal, as assayed by an independently collected measure of fear potentiated startle. Collectively, our finding suggests that development of PTSD is associated with threat-related decreases in hippocampal function because of increases in fear-potentiated arousal.

AB - Hippo campal impairments are reliably associated with post-traumatic stress disorder (PTSD); however, little research has characterized how increased threat sensitivity may interact with arousal responses to alter hippocampal reactivity, and further how these interactions relate to the sequelae of trauma-related symptoms. In a sample of individuals recently exposed to trauma (N = 116, 76 female), we found that PTSD symptoms at 2 weeks were associated with decreased hippocampal responses to threat as assessed with fMRI. Further, the relationship between hippocampal threat sensitivity and PTSD symptomology only emerged in individuals who showed transient, high threat-related arousal, as assayed by an independently collected measure of fear potentiated startle. Collectively, our finding suggests that development of PTSD is associated with threat-related decreases in hippocampal function because of increases in fear-potentiated arousal.

KW - arousal

KW - fMRI

KW - fear

KW - hippocampus

KW - trauma

UR - http://www.scopus.com/inward/record.url?scp=85137386523&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.0838-22.2022

DO - 10.1523/JNEUROSCI.0838-22.2022

M3 - Article

C2 - 35840324

AN - SCOPUS:85137386523

SN - 0270-6474

VL - 42

SP - 6593

EP - 6604

JO - Journal of Neuroscience

JF - Journal of Neuroscience

IS - 34

ER -

Hippocampal Threat Reactivity Interacts with Physiological Arousal to Predict PTSD Symptoms

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Keywords

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