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European Journal of Psychotraumatology Volume 15, 2024 - Issue 1
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Basic Research Article

Circulating PACAP levels are associated with altered imaging measures of entorhinal cortex neurite density in posttraumatic stress disorder

Los niveles circulantes del PACAP están asociados con medidas de imagen alteradas de la densidad de neuritas de la corteza entorrinal en el trastorno de estrés postraumático

Steven J. Grangera Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USA;b Department of Psychiatry, Harvard Medical School, Boston, MA, USACorrespondence[email protected]
View further author information
,
Victor Mayc Larner College of Medicine, University of Vermont, Burlington, VT, USAView further author information
,
Sayamwong E. Hammackc Larner College of Medicine, University of Vermont, Burlington, VT, USAView further author information
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Eylül Akmana Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USAView further author information
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Sydney A. Jobsona Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USAView further author information
,
Elizabeth A. Olsona Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USA;b Department of Psychiatry, Harvard Medical School, Boston, MA, USAView further author information
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Cameron D. Perniaa Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USA;b Department of Psychiatry, Harvard Medical School, Boston, MA, USA;d Basic Neuroscience Division, McLean Hospital, Belmont, MA, USA;e Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USAView further author information
,
Nikos P. Daskalakisa Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USA;b Department of Psychiatry, Harvard Medical School, Boston, MA, USA;d Basic Neuroscience Division, McLean Hospital, Belmont, MA, USA;e Stanley Center for Psychiatric Research, Broad Institute of MIT and Harvard, Cambridge, MA, USAView further author information
,
Caitlin Ravichandrana Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USA;f Department of Pediatrics, Harvard Medical School, Boston, MA, USA;g Lurie Center for Autism, Massachusetts General Hospital, Lexington, MA, USAView further author information
,
William A. Carlezon Jr.d Basic Neuroscience Division, McLean Hospital, Belmont, MA, USA;f Department of Pediatrics, Harvard Medical School, Boston, MA, USAView further author information
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Kerry J. Resslera Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USA;b Department of Psychiatry, Harvard Medical School, Boston, MA, USAView further author information
,
Scott L. Raucha Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USA;b Department of Psychiatry, Harvard Medical School, Boston, MA, USAView further author information
&
Isabelle M. Rossoa Division of Depression and Anxiety Disorders, McLean Hospital, Belmont, MA, USA;b Department of Psychiatry, Harvard Medical School, Boston, MA, USAView further author information
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Article: 2335793 | Received 29 Sep 2023, Accepted 18 Mar 2024, Published online: 08 Apr 2024

References

  • Abraham, A., Pedregosa, F., Eickenberg, M., Gervais, P., Mueller, A., Kossaifi, J., Gramfort, A., Thirion, B., & Varoquaux, G. (2014). Machine learning for neuroimaging with scikit-learn. Frontiers in Neuroinformatics, 8, 14. https://doi.org/10.3389/fninf.2014.00014
  • Agarwal, A., Halvorson, L. M., & Legradi, G. (2005). Pituitary adenylate cyclase-activating polypeptide (PACAP) mimics neuroendocrine and behavioral manifestations of stress: Evidence for PKA-mediated expression of the corticotropin-releasing hormone (CRH) gene. Molecular Brain Research, 138(1), 45–57. https://doi.org/10.1016/j.molbrainres.2005.03.016
  • Almli, L. M., Mercer, K. B., Kerley, K., Feng, H., Bradley, B., Conneely, K. N., & Ressler, K. J. (2013). ADCYAP1R1 genotype associates with post-traumatic stress symptoms in highly traumatized African-American females. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 162(3), 262–272. https://doi.org/10.1002/ajmg.b.32145
  • Amaral, D., & Lavenex, P. (2007). Hippocampal neuroanatomy. In P. Andersen, R. Morris, D. Amaral, T. Bliss, & J. O’Keefe (Eds.), The hippocampus book (pp. 37–114). Oxford University Press.
  • Andersson, J. L. R., Graham, M. S., Zsoldos, E., & Sotiropoulos, S. N. (2016). Incorporating outlier detection and replacement into a non-parametric framework for movement and distortion correction of diffusion MR images. NeuroImage, 141, 556–572. https://doi.org/10.1016/j.neuroimage.2016.06.058
  • Andersson, J. L., Skare, S., & Ashburner, J. (2003). How to correct susceptibility distortions in spin-echo echo-planar images: Application to diffusion tensor imaging. NeuroImage, 20(2), 870–888. https://doi.org/10.1016/S1053-8119(03)00336-7
  • Andersson, J. L. R., & Sotiropoulos, S. N. (2016). An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. NeuroImage, 125, 1063–1078. https://doi.org/10.1016/j.neuroimage.2015.10.019
  • Armour, C., Elhai, J. D., Richardson, D., Ractliffe, K., Wang, L., & Elklit, A. (2012). Assessing a five factor model of PTSD: Is dysphoric arousal a unique PTSD construct showing differential relationships with anxiety and depression? Journal of Anxiety Disorders, 26(2), 368–376. https://doi.org/10.1016/j.janxdis.2011.12.002
  • Avants, B. B., Tustison, N., & Song, G. (2009). Advanced normalization tools (ANTS). The Insight Journal, 2, 1–35.
  • Bastiani, M., Cottaar, M., Fitzgibbon, S. P., Suri, S., Alfaro-Almagro, F., Sotiropoulos, S. N., Jbabdi, S., & Andersson, J. L. R. (2019). Automated quality control for within and between studies diffusion MRI data using a non-parametric framework for movement and distortion correction. NeuroImage, 184, 801–812. https://doi.org/10.1016/j.neuroimage.2018.09.073
  • Ben-Zion, Z., Zeevi, Y., Keynan, N. J., Admon, R., Kozlovski, T., Sharon, H., Halpern, P., Liberzon, I., Shalev, A. Y., Benjamini, Y., & Hendler, T. (2020). Multi-domain potential biomarkers for post-traumatic stress disorder (PTSD) severity in recent trauma survivors. Translational Psychiatry, 10(1), 208. https://doi.org/10.1038/s41398-020-00898-z
  • Boucher, M. N., May, V., Braas, K. M., & Hammack, S. E. (2021). PACAP orchestration of stress-related responses in neural circuits. Peptides, 142, 170554. https://doi.org/10.1016/j.peptides.2021.170554
  • Chang, S. C., Xie, P., Anton, R. F., De Vivo, I., Farrer, L. A., Kranzler, H. R., Oslin, D., Purcell, S. M., Roberts, A. L., Smoller, J. W., Uddin, M., Gelernter, J., & Koenen, K. C. (2012). No association between ADCYAP1R1 and post-traumatic stress disorder in two independent samples. Molecular Psychiatry, 17(3), 239–241. https://doi.org/10.1038/mp.2011.118
  • Clancy, K. J., Devignes, Q., Kumar, P., May, V., Hammack, S. E., Akman, E., Pernia, C. D., Jobson, S. A., Lewis, M. W., Daskalakis, N. P., Carlezon, W. A., Ressler, K. J., Rauch, S. L., & Rosso, I. M. (2023). Circulating PACAP levels are associated with increased amygdala-default mode network resting-state connectivity in posttraumatic stress disorder. Neuropsychopharmacology, 48(8), 1245–1254. https://doi.org/10.1038/s41386-023-01593-5
  • Condro, M. C., Matynia, A., Foster, N. N., Ago, Y., Rajbhandari, A. K., Van, C., Jayaram, B., Parikh, S., Diep, A. L., Nguyen, E., May, V., Dong, H., & Waschek, J. A. (2016). High-resolution characterization of a PACAP-EGFP transgenic mouse model for mapping PACAP-expressing neurons. Journal of Comparative Neurology, 524(18), 3827–3848. https://doi.org/10.1002/cne.24035
  • Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162–173. https://doi.org/10.1006/cbmr.1996.0014
  • Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179–194. https://doi.org/10.1006/nimg.1998.0395
  • Feng, H., Su, J., Fang, W., Chen, X., & He, J. (2021). The entorhinal cortex modulates trace fear memory formation and neuroplasticity in the mouse lateral amygdala via cholecystokinin. eLife, 10, e69333. https://doi.org/10.7554/eLife.69333
  • Foilb, A. R., Taylor-Yeremeeva, E. M., Fritsch, E. L., Ravichandran, C., Lezak, K. R., Missig, G., McCullough, K. M., & Carlezon, W. A., Jr. (2024). Differential effects of the stress peptides PACAP and CRF on sleep architecture in mice. NPP-Digital Psychiatry and Neuroscience, in press. Retrieved February 7, 2024.
  • Granger, S. J., Colon-Perez, L., Larson, M. S., Phelan, M., Keator, D. B., Janecek, J. T., Sathishkumar, M. T., Smith, A. P., McMillan, L., Greenia, D., Corrada, M. M., Kawas, C. H., & Yassa, M. A. (2022). Hippocampal dentate gyrus integrity revealed with ultrahigh resolution diffusion imaging predicts memory performance in older adults. Hippocampus, 32(9), 627–638. https://doi.org/10.1002/hipo.23456
  • Hammack, S. E., & May, V. (2015). Pituitary adenylate cyclase activating polypeptide in stress-related disorders: Data convergence from animal and human studies. Biological Psychiatry, 78(3), 167–177. https://doi.org/10.1016/j.biopsych.2014.12.003
  • Harms, R. L., Fritz, F. J., Tobisch, A., Goebel, R., & Roebroeck, A. (2017). Robust and fast nonlinear optimization of diffusion MRI microstructure models. NeuroImage, 155, 82–96. https://doi.org/10.1016/j.neuroimage.2017.04.064
  • Hashimoto, H., Nogi, H., Mori, K., Ohishi, H., Shigemoto, R., Yamamoto, K., Matsuda, T., Mizuno, N., Nagata, S., & Baba, A. (1996). Distribution of the mRNA for a pituitary adenylate cyclase-activating polypeptide receptor in the rat brain: An in situ hybridization study. The Journal of Comparative Neurology, 371(4), 567–577.
  • Hashimoto, H., Shintani, N., Tanida, M., Hayata, A., Hashimoto, R., & Baba, A. (2011). PACAP is implicated in the stress axes. Current Pharmaceutical Design, 17(10), 985–989. https://doi.org/10.2174/138161211795589382
  • Hisey, E., Purkey, A., Gao, Y., Hossain, K., Soderling, S. H., & Ressler, K. J. (2023). A ventromedial prefrontal-to-lateral entorhinal cortex pathway modulates the gain of behavioral responding during threat. Biological Psychiatry, 94(3), 239–248. https://doi.org/10.1016/j.biopsych.2023.01.009
  • Hunsaker, M. R., Chen, V., Tran, G. T., & Kesner, R. P. (2013). The medial and lateral entorhinal cortex both contribute to contextual and item recognition memory: A test of the binding ofitems and context model. Hippocampus, 23(5), 380–391. https://doi.org/10.1002/hipo.22097
  • Jaworski, D. M., & Proctor, M. D. (2000). Developmental regulation of pituitary adenylate cyclase-activating polypeptide and PAC1 receptor mRNA expression in the rat central nervous system. Developmental Brain Research, 120(1), 27–39. https://doi.org/10.1016/S0165-3806(99)00192-3
  • Johnson, G. C., Parsons, R., May, V., & Hammack, S. E. (2020). The role of pituitary adenylate cyclase-activating polypeptide (PACAP) signaling in the hippocampal dentate gyrus. Frontiers in Cellular Neuroscience, 14, 111. https://doi.org/10.3389/fncel.2020.00111
  • Kamiya, K., Hori, M., & Aoki, S. (2020). NODDI in clinical research. Journal of Neuroscience Methods, 346, 108908. https://doi.org/10.1016/j.jneumeth.2020.108908
  • Kang, M. S., & Han, J. H. (2021). Optogenetic inhibition of medial entorhinal cortex inputs to the hippocampus during a short period of time right after learning disrupts contextual fear memory formation. Molecular Brain, 14(2), https://doi.org/10.1186/s13041-020-00719-w
  • Kondo, T., Tominaga, T., Ichikawa, M., & Iijima, T. (1997). Differential alteration of hippocampal synaptic strength induced by pituitary adenylate cyclase activating polypeptide-38 (PACAP-38). Neuroscience Letters, 221(2-3), 189–192. https://doi.org/10.1016/S0304-3940(96)13323-1
  • Lopez, K. C., Leary, J. B., Pham, D. L., Chou, Y. Y., Dsurney, J., & Chan, L. (2017). Brain volume, connectivity, and neuropsychological performance in mild traumatic brain injury: The impact of post-traumatic stress disorder symptoms. Journal of Neurotrauma, 34(1), 16–22. https://doi.org/10.1089/neu.2015.4323
  • Luo, D., Ganesh, S., & Koolaard, J. (2023). Predictmeans: Predicted means for linear and semiparametric models. https://CRAN.R-project.org/package=predictmeans
  • Lucignani, M., Breschi, L., Espagnet, M. C. R., Longo, D., Talamanca, L. F., Placidi, E., & Napolitano, A. (2021). Reliability on multiband diffusion NODDI models: A test retest study on children and adults. NeuroImage, 238, 118234. https://doi.org/10.1016/j.neuroimage.2021.118234
  • Matsuyama, S., Matsumoto, A., Hashimoto, H., Shintani, N., & Baba, A. (2003). Impaired long-term potentiation in vivo in the dentate gyrus of pituitary adenylate cyclase-activating polypeptide (PACAP) or PACAP type 1 receptor-mutant mice. Neuroreport, 14(16), 2095–2098. https://doi.org/10.1097/00001756-200311140-00017
  • Meloni, E. G., Kaye, K. T., Venkataraman, A., & Carlezon, W. A. Jr. (2019). PACAP increases Arc/Arg 3.1 expression within the extended amygdala after fear conditioning in rats. Neurobiology of Learning and Memory, 157, 24–34. https://doi.org/10.1016/j.nlm.2018.11.011
  • Meloni, E. G., Venkataraman, A., Donahue, R. J., & Carlezon, W. A. Jr. (2016). Bi-directional effects of pituitary adenylate cyclase-activating polypeptide (PACAP) on fear-related behavior and c-Fos expression after fear conditioning in rats. Psychoneuroendocrinology, 64, 12–21. https://doi.org/10.1016/j.psyneuen.2015.11.003
  • Merenstein, J. L., Zhao, J., Mullin, H. A., Rudolph, M. D., Song, A. W., & Madden, D. J. (2023). High-resolution multi-shot diffusion imaging of structural networks in healthy neurocognitive aging. NeuroImage, 275, 120191. https://doi.org/10.1016/j.neuroimage.2023.120191
  • Missig, G., Roman, C. W., Vizzard, M. A., Braas, K. M., Hammack, S. E., & May, V. (2014). Parabrachial nucleus (PBn) pituitary adenylate cyclase activating polypeptide (PACAP) signaling in the amygdala: Implication for the sensory and behavioral effects of pain. Neuropharmacology, 86, 38–48. https://doi.org/10.1016/j.neuropharm.2014.06.022
  • Mo, X., He, M., Zhou, L., Liu, Y., Zhu, H., Huang, X., Zeng, G., Zhang, J., & Li, L. (2022). Mapping structural covariance networks in children and adolescents with post-traumatic stress disorder after earthquake. Frontiers in Psychiatry, 13, 923572. https://doi.org/10.3389/fpsyt.2022.923572
  • Mueller-Pfeiffer, C., Schick, M., Schulte-Vels, T., O’Gorman, R., Michels, L., Martin-Soelch, C., Blair, J. R., Rufer, M., Schnyder, U., Zeffiro, T., & Hasler, G. (2013). Atypical visual processing in posttraumatic stress disorder. NeuroImage: Clinical, 3, 531–538. https://doi.org/10.1016/j.nicl.2013.08.009
  • Nazeri, A., Chakravarty, M. M., Rotenberg, D. J., Rajji, T. K., Rathi, Y., Michailovich, O. V., & Voineskos, A. N. (2015). Functional consequences of neurite orientation dispersion and density in humans across the adult lifespan. The Journal of Neuroscience, 35(4), 1753–1762. https://doi.org/10.1523/JNEUROSCI.3979-14.2015
  • Ogata, K., Shintani, N., Hayata-Takano, A., Kamo, T., Higashi, S., Seiriki, K., Momosaki, H., Vaudry, D., Vaudry, H., Galas, L., Kasai, A., Nagayasu, K., Nakazawa, T., Hashimoto, R., Ago, Y., Matsuda, T., Baba, A., & Hashimoto, H. (2015). PACAP enhances axon outgrowth in cultured hippocampal neurons to a comparable extent as BDNF. PLoS One, 10, e0120526. https://doi.org/10.1371/journal.pone.0120526
  • Olman, C. A., Davachi, L., & Inati, S. (2009). Distortion and signal loss in medial temporal lobe. PLoS One, 4(12), e8160. https://doi.org/10.1371/journal.pone.0008160
  • Otto, C., Kovalchuk, Y., Wolfer, D. P., Gass, P., Martin, M., Zuschratter, W., Gröne, H. J., Kellendonk, C., Tronche, F., Maldonado, R., Lipp, H.-P., Konnerth, A., & Schütz, G. (2001). Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. The Journal of Neuroscience, 21(15), 5520–5527. https://doi.org/10.1523/JNEUROSCI.21-15-05520.2001
  • Palkovits, M., Somogyvári-Vigh, A., & Arimura, A. (1995). Concentrations of pituitary adenylate cyclase activating polypeptide (PACAP) in human brain nuclei. Brain Research, 699(1), 116–120. https://doi.org/10.1016/0006-8993(95)00869-R
  • Parvathaneni, P., Nath, V., Blaber, J. A., Schilling, K. G., Hainline, A. E., Mojahed, E., Anderson, A. W., & Landman, B. A. (2018). Empirical reproducibility, sensitivity, and optimization of acquisition protocol, for Neurite Orientation Dispersion and Density Imaging using AMICO. Magnetic Resonance Imaging, 50, 96–109. https://doi.org/10.1016/j.mri.2018.03.004
  • Piggins, H. D., Stamp, J. A., Burns, J., Rusak, B., & Semba, K. (1996). Distribution of pituitary adenylate cyclase activating polypeptide (PACAP) immunoreactivity in the hypothalamus and extended amygdala of the rat. The Journal of Comparative Neurology, 376(2), 278–294. https://doi.org/10.1002/(SICI)1096-9861(19961209)376:2<278::AID-CNE9>3.0.CO;2-0
  • Porta-Casteràs, D., Cano, M., Steward, T., Andero, R., & Cardoner, N. (2022). The pituitary adenylate cyclase-activating polypeptide system as a sex-specific modulator of hippocampal response to threat stimuli. Neurobiology of Stress, 18, 100448. https://doi.org/10.1016/j.ynstr.2022.100448
  • Radhakrishnan, H., Bennett, I. J., & Stark, C. E. (2022). Higher-order multi-shell diffusion measures complement tensor metrics and volume in gray matter when predicting age and cognition. NeuroImage, 253, 119063. https://doi.org/10.1016/j.neuroimage.2022.119063
  • Radhakrishnan, H., Shabestari, S. K., Blurton-Jones, M., Obenaus, A., & Stark, C. E. L. (2022). Using advanced diffusion-weighted imaging to predict cell counts in gray matter: Potential and pitfalls. Frontiers in Neuroscience, 16, 881713. https://doi.org/10.3389/fnins.2022.881713
  • Radhakrishnan, H., Stark, S. M., & Stark, C. E. L. (2020). Microstructural alterations in hippocampal subfields mediate age-related memory decline in humans. Frontiers in Aging Neuroscience, 12, 94. https://doi.org/10.3389/fnagi.2020.00094
  • Reagh, Z. M., & Yassa, M. A. (2014). Object and spatial mnemonic interference differentially engage lateral and medial entorhinal cortex in humans. Proceedings of the National Academy of Sciences, 111(40), E4264–E4273. https://doi.org/10.1073/pnas.1411250111
  • Ressler, K. J., Berretta, S., Bolshakov, V. Y., Rosso, I. M., Meloni, E. G., Rauch, S. L., & Carlezon, W. A., Jr. (2022). Post-traumatic stress disorder: Clinical and translational neuroscience from cells to circuits. Nature Reviews Neurology, 18(5), 273–288. https://doi.org/10.1038/s41582-022-00635-8
  • Ressler, K. J., Mercer, K. B., Bradley, B., Jovanovic, T., Mahan, A., Kerley, K., Norrholm, S. D., Kilaru, V., Smith, A. K., Myers, A. J., Ramirez, M., Engel, A., Hammack, S. E., Toufexis, D., Braas, K. M., Binder, E. B., & May, V. (2011). Post-traumatic stress disorder is associated with PACAP and the PAC1 receptor. Nature, 470(7335), 492–497. https://doi.org/10.1038/nature09856
  • Ritchey, M., Libby, L. A., & Ranganath, C. (2015). Progress in brain research. Progress in Brain Research, 219, 45–64. https://doi.org/10.1016/bs.pbr.2015.04.001
  • Rivnyak, A., Kiss, P., Tamas, A., Balogh, D., & Reglodi, D. (2018). Review on PACAP-induced transcriptomic and proteomic changes in neuronal development and repair. International Journal of Molecular Sciences, 19(4), 1020. https://doi.org/10.3390/ijms19041020
  • Roesler, R., & McGaugh, J. L. (2022). The entorhinal cortex as a gateway for amygdala influences on memory consolidation. Neuroscience, 497, 86–96. https://doi.org/10.1016/j.neuroscience.2022.01.023
  • Ross, R. A., Hoeppner, S. S., Hellberg, S. N., O’Day, E. B., Rosencrans, P. L., Ressler, K. J., May, V., & Simon, N. M. (2020). Circulating PACAP peptide and PAC1R genotype as possible transdiagnostic biomarkers for anxiety disorders in women: A preliminary study. Neuropsychopharmacology, 45(7), 1125–1133. https://doi.org/10.1038/s41386-020-0604-4
  • Rosso, I. M., Crowley, D. J., Silveri, M. M., Rauch, S. L., & Jensen, J. E. (2017). Hippocampus glutamate and N-acetyl aspartate markers of excitotoxic neuronal compromise in posttraumatic stress disorder. Neuropsychopharmacology, 42(8), 1698–1705. https://doi.org/10.1038/npp.2017.32
  • Schmidt, S. D., Myskiw, J. C., Furini, C. R., Schmidt, B. E., Cavalcante, L. E., & Izquierdo, I. (2015). PACAP modulates the consolidation and extinction of the contextual fear conditioning through NMDA receptors. Neurobiology of Learning and Memory, 118, 120–124. https://doi.org/10.1016/j.nlm.2014.11.014
  • Schultz, H., Sommer, T., & Peters, J. (2012). Direct evidence for domain-sensitive functional subregions in human entorhinal cortex. The Journal of Neuroscience, 32(14), 4716–4723. https://doi.org/10.1523/JNEUROSCI.5126-11.2012
  • Shin, L. M., Rauch, S. L., & Pitman, R. K. (2006). Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Annals of the New York Academy of Sciences, 1071(1), 67–79. https://doi.org/10.1196/annals.1364.007
  • Shneider, Y., Shtrauss, Y., Yadid, G., & Pinhasov, A. (2010). Differential expression of PACAP receptors in postnatal rat brain. Neuropeptides, 44(6), 509–514. https://doi.org/10.1016/j.npep.2010.09.001
  • Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., Bannister, P. R., De Luca, M., Drobnjak, I., Flitney, D. E., Niazy, R. K., Saunders, J., Vickers, J., Zhang, Y., De Stefano, N., Brady, J. M., & Matthews, P. M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23 Suppl 1, S208–S219. https://doi.org/10.1016/j.neuroimage.2004.07.051
  • Sparta, D. R., Smithuis, J., Stamatakis, A. M., Jennings, J. H., Kantak, P. A., Ung, R. L., & Stuber, G. D. (2014). Inhibition of projections from the basolateral amygdala to the entorhinal cortex disrupts the acquisition of contextual fear. Frontiers in Behavioral Neuroscience, 8, 129. https://doi.org/10.3389/fnbeh.2014.00129
  • Stevens, J. S., Almli, L. M., Fani, N., Gutman, D. A., Bradley, B., Norrholm, S. D., Reiser, E., Ely, T. D., Dhanani, R., Glover, E. M., Jovanovic, T., & Ressler, K. J. (2014). PACAP receptor gene polymorphism impacts fear responses in the amygdala and hippocampus. Proceedings of the National Academy of Sciences, 111(8), 3158–3163. https://doi.org/10.1073/pnas.1318954111
  • Stroth, N., & Eiden, L. E. (2010). Stress hormone synthesis in mouse hypothalamus and adrenal gland triggered by restraint is dependent on pituitary adenylate cyclase-activating polypeptide signaling. Neuroscience, 165(4), 1025–1030. https://doi.org/10.1016/j.neuroscience.2009.11.023
  • Uddin, M., Chang, S. C., Zhang, C., Ressler, K., Mercer, K. B., Galea, S., Keyes, K. M., McLaughlin, K. A., Wildman, D. E., Aiello, A. E., & Koenen, K. C. (2013). ADCYAP1R1 genotype, posttraumatic stress disorder, and depression among women exposed to childhood maltreatment. Depression and Anxiety, 30(3), 251–258. https://doi.org/10.1002/da.22037
  • Wang, L., Cao, C., Wang, R., Qing, Y., Zhang, J., & Zhang, X. Y. (2013). PAC1 receptor (ADCYAP1R1) genotype is associated with PTSD’s emotional numbing symptoms in Chinese earthquake survivors. Journal of Affective Disorders, 150(1), 156–159. https://doi.org/10.1016/j.jad.2013.01.010
  • Warnes, G. R., Bolker, B., Lumley, T., from Randall C. Johnson are Copyright SAIC-Frederick, R. C. Johnson. C., by the Intramural Research Program, Inc. F., of the NIH, Institute, N. C., & for Cancer Research under NCI Contract NO1-CO-12400., C. (2022). gmodels: Various R Programming Tools for Model Fitting. https://CRAN.R-project.org/package=gmodels
  • Weathers, F. W., Bovin, M. J., Lee, D. J., Sloan, D. M., Schnurr, P. P., Kaloupek, D. G., Keane, T. M., & Marx, B. P. (2018). The clinician-administered PTSD scale for DSM-5 (CAPS-5): development and initial psychometric evaluation in military veterans. Psychological Assessment, 30(3), 383–395. https://doi.org/10.1037/pas0000486
  • Witter, M. P., & Amaral, D. G. (1991). Entorhinal cortex of the monkey: V. Projections to the dentate gyrus, hippocampus, and subicular complex. Journal of Comparative Neurology, 307(3), 437–459. https://doi.org/10.1002/cne.903070308
  • Witter, M. P., Doan, T. P., Jacobsen, B., Nilssen, E. S., & Ohara, S. (2017). Architecture of the entorhinal cortex A review of entorhinal anatomy in rodents with some comparative notes. Frontiers in Systems Neuroscience, 11, 46. https://doi.org/10.3389/fnsys.2017.00046
  • Yassa, M. A., & Stark, C. E. (2011). Pattern separation in the hippocampus. Trends in Neurosciences, 34(10), 515–525. https://doi.org/10.1016/j.tins.2011.06.006
  • Yi, S. Y., Barnett, B. R., Torres-Velázquez, M., Zhang, Y., Hurley, S. A., Rowley, P. A., Hernando, D., & Yu, J.-P. J. (2019). Detecting microglial density with quantitative multi-compartment diffusion MRI. Frontiers in Neuroscience, 13, 81. https://doi.org/10.3389/fnins.2019.00081
  • Zhang, H., Schneider, T., Wheeler-Kingshott, C. A., & Alexander, D. C. (2012). NODDI: Practical in vivo neurite orientation dispersion and density imaging of the human brain. NeuroImage, 61(4), 1000–1016. https://doi.org/10.1016/j.neuroimage.2012.03.072

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