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Published in: BMC Psychiatry 1/2018

Open Access 01-12-2018 | Research article

Functional connectivity of hippocampal subregions in PTSD: relations with symptoms

Authors: Bailee L. Malivoire, Todd A. Girard, Ronak Patel, Candice M. Monson

Published in: BMC Psychiatry | Issue 1/2018

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Abstract

Background

Posttraumatic stress disorder (PTSD) is associated with abnormal hippocampal activity; however, the functional connectivity (FC) of the hippocampus with other brain regions in PTSD and its relations with symptoms warrants further attention. We investigated subregional hippocampal FC in PTSD during a resting state compared with a trauma-exposed control (TEC) group. Based on extant research, we targeted the FCs of the anterior and posterior hippocampal subregions with the amygdala, medial prefrontal cortex (mPFC), and the posterior cingulate (PCC).

Methods

Resting-state functional magnetic resonance images were acquired from 11 individuals with PTSD and 13 trauma-exposed controls. Anterior and posterior hippocampal FC was compared between groups. Within the PTSD and TEC groups, subregional hippocampal FC was correlated with scores on the Clinician-Administered PTSD Scale (CAPS) at time of scan and 4 months post-scan.

Results

Those with PTSD had significantly greater FC compared with the TEC group between the left posterior hippocampus and the bilateral PCC (g’s > .96). Direct contrasts of the Fisher z-transformed coefficients indicated that the correlations between CAPS scores 4 months post scan and the FC between the left hippocampal head and the right PCC (z = − 2.07, p = .039) as well as the FC between the right hippocampal tail and the right mPFC (z = − 2.19, p = .029) were significantly greater in the PTSD group compared to the TEC group.

Conclusions

These results support between-group differences in posterior hippocampal FC and different relations with PTSD future symptoms, underscoring associations with the anterior and posterior hippocampus. These findings enrich our understanding of PTSD pathophysiology and provide support for future investigations of imaging biomarkers predictive of disease progression.
Literature
1.
go back to reference American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th ed. Arlington: American Psychiatric Publishing; 2013.CrossRef American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th ed. Arlington: American Psychiatric Publishing; 2013.CrossRef
2.
go back to reference Patel R, Spreng RN, Shin LM, Girard TA. Neurocircuitry models of posttraumatic stress disorder and beyond: a meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev. 2012;36:2130–42.CrossRefPubMed Patel R, Spreng RN, Shin LM, Girard TA. Neurocircuitry models of posttraumatic stress disorder and beyond: a meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev. 2012;36:2130–42.CrossRefPubMed
3.
go back to reference Stark EA, Parsons CE, Van Hartevelt TJ, Charquero-Ballester M, McManners H, Ehlers A, et al. Post-traumatic stress influences the brain even in the absence of symptoms: a systematic, quantitative meta-analysis of neuroimaging studies. Neurosci Biobehav Rev. 2015;56:207–21.CrossRefPubMed Stark EA, Parsons CE, Van Hartevelt TJ, Charquero-Ballester M, McManners H, Ehlers A, et al. Post-traumatic stress influences the brain even in the absence of symptoms: a systematic, quantitative meta-analysis of neuroimaging studies. Neurosci Biobehav Rev. 2015;56:207–21.CrossRefPubMed
4.
go back to reference Rauch SL, Shin LM, Phelps EA. Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research—past, present, and future. Biol Psychiatry. 2006;60:376–82.CrossRefPubMed Rauch SL, Shin LM, Phelps EA. Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research—past, present, and future. Biol Psychiatry. 2006;60:376–82.CrossRefPubMed
5.
go back to reference Rauch SL, Shin LM, Whalen PJ, Pitman RK. Neuroimaging and the neuroanatomy of PTSD. CNS Spectr. 1998;3:30–41.CrossRef Rauch SL, Shin LM, Whalen PJ, Pitman RK. Neuroimaging and the neuroanatomy of PTSD. CNS Spectr. 1998;3:30–41.CrossRef
6.
go back to reference Fornito A, Bullmore ET. What can spontaneous fluctuations of the blood oxygenation-level-dependent signal tell us about psychiatric disorders? Curr Opin Psychiatry. 2010;23:239–49.CrossRefPubMed Fornito A, Bullmore ET. What can spontaneous fluctuations of the blood oxygenation-level-dependent signal tell us about psychiatric disorders? Curr Opin Psychiatry. 2010;23:239–49.CrossRefPubMed
7.
go back to reference Fox MD, Greicius M. Clinical applications of resting state functional connectivity. Front Syst Neurosci. 2010;4:1–13. Fox MD, Greicius M. Clinical applications of resting state functional connectivity. Front Syst Neurosci. 2010;4:1–13.
8.
go back to reference Brewin CR, Gregory JD, Lipton M, Burgess N. Intrusive images in psychological disorders: characteristics, neural mechanisms, and treatment implications. Psychol Rev. 2010;117:210–32.CrossRefPubMedPubMedCentral Brewin CR, Gregory JD, Lipton M, Burgess N. Intrusive images in psychological disorders: characteristics, neural mechanisms, and treatment implications. Psychol Rev. 2010;117:210–32.CrossRefPubMedPubMedCentral
9.
go back to reference Carrion VG, Wong SS. Can traumatic stress alter the brain? Understanding the implications of early trauma on brain development and learning. J Adolesc Health. 2012;51:23–8.CrossRef Carrion VG, Wong SS. Can traumatic stress alter the brain? Understanding the implications of early trauma on brain development and learning. J Adolesc Health. 2012;51:23–8.CrossRef
10.
go back to reference Bremner JD, Vermetten E, Afzal N, Vythilingam M. Deficits in verbal declarative memory function in women with childhood sexual abuse-related posttraumatic stress disorder. J Nerv Ment Dis. 2004;192:643–9.CrossRefPubMed Bremner JD, Vermetten E, Afzal N, Vythilingam M. Deficits in verbal declarative memory function in women with childhood sexual abuse-related posttraumatic stress disorder. J Nerv Ment Dis. 2004;192:643–9.CrossRefPubMed
11.
go back to reference Vasterling JJ, Duke LM, Brailey K, Constans JI, Allain AN, Sutker PB. Attention, learning, and memory performances and intellectual resources in Vietnam veterans: PTSD and no disorder comparisons. Neuropsychology. 2002;16:5–14.CrossRefPubMed Vasterling JJ, Duke LM, Brailey K, Constans JI, Allain AN, Sutker PB. Attention, learning, and memory performances and intellectual resources in Vietnam veterans: PTSD and no disorder comparisons. Neuropsychology. 2002;16:5–14.CrossRefPubMed
12.
go back to reference Bremner JD, Scott TM, Delaney RC, Southwick SM, Mason JW, Johnson DR, et al. Deficits in short-term memory in posttraumatic stress disorder. Am J Psychiatr. 1993;150:1015–9.CrossRefPubMed Bremner JD, Scott TM, Delaney RC, Southwick SM, Mason JW, Johnson DR, et al. Deficits in short-term memory in posttraumatic stress disorder. Am J Psychiatr. 1993;150:1015–9.CrossRefPubMed
13.
go back to reference Yehuda R, Keefe RS, Harvey PD, Levengood RA. Learning and memory in combat veterans with posttraumatic stress disorder. Am J Psychiatry. 1995;152:137–9.CrossRefPubMed Yehuda R, Keefe RS, Harvey PD, Levengood RA. Learning and memory in combat veterans with posttraumatic stress disorder. Am J Psychiatry. 1995;152:137–9.CrossRefPubMed
14.
go back to reference Greicius M. Resting-state functional connectivity in neuropsychiatric disorders. Curr Opin Neurol. 2008;21:424–30.CrossRefPubMed Greicius M. Resting-state functional connectivity in neuropsychiatric disorders. Curr Opin Neurol. 2008;21:424–30.CrossRefPubMed
15.
go back to reference Jin C, Qi R, Yin Y, Hu X, Duan L, Xu Q, et al. Abnormalities in whole-brain functional connectivity observed in treatment-naive post-traumatic stress disorder patients following an earthquake. Psychol Med. 2014;44:1927–36.CrossRefPubMed Jin C, Qi R, Yin Y, Hu X, Duan L, Xu Q, et al. Abnormalities in whole-brain functional connectivity observed in treatment-naive post-traumatic stress disorder patients following an earthquake. Psychol Med. 2014;44:1927–36.CrossRefPubMed
16.
go back to reference Bluhm RL, Williamson PC, Osuch EA, Frewen PA, Stevens TK, Boksman K, Lanius RA. Alterations in default network connectivity in posttraumatic stress disorder related to early-life trauma. J Psychiatry Neurosci. 2009;34:187–94.PubMedPubMedCentral Bluhm RL, Williamson PC, Osuch EA, Frewen PA, Stevens TK, Boksman K, Lanius RA. Alterations in default network connectivity in posttraumatic stress disorder related to early-life trauma. J Psychiatry Neurosci. 2009;34:187–94.PubMedPubMedCentral
17.
go back to reference Sripada RK, King AP, Garfinkel SN, Wang X, Sripada CS, Welsh RC, Liberzon I. Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder. J Psychiatry Neurosci. 2012;37:241–9.CrossRefPubMedPubMedCentral Sripada RK, King AP, Garfinkel SN, Wang X, Sripada CS, Welsh RC, Liberzon I. Altered resting-state amygdala functional connectivity in men with posttraumatic stress disorder. J Psychiatry Neurosci. 2012;37:241–9.CrossRefPubMedPubMedCentral
18.
go back to reference Zhang X, Zhang J, Wang L, Li R, Zhang W. Altered resting-state functional connectivity of the amygdala in Chinese earthquake survivors. Prog Neuro-Psychopharmacol Biol Psychiatry. 2016;65:208–14.CrossRef Zhang X, Zhang J, Wang L, Li R, Zhang W. Altered resting-state functional connectivity of the amygdala in Chinese earthquake survivors. Prog Neuro-Psychopharmacol Biol Psychiatry. 2016;65:208–14.CrossRef
19.
go back to reference Zhou Y, Wang Z, Qin L, Wan J, Sun Y, Su S, et al. Early altered resting-state functional connectivity predicts the severity of post-traumatic stress disorder symptoms in acutely traumatized subjects. PLoS One. 2012;7:1–6. Zhou Y, Wang Z, Qin L, Wan J, Sun Y, Su S, et al. Early altered resting-state functional connectivity predicts the severity of post-traumatic stress disorder symptoms in acutely traumatized subjects. PLoS One. 2012;7:1–6.
20.
go back to reference Chen AC, Etkin A. Hippocampal network connectivity and activation differentiates post-traumatic stress disorder from generalized anxiety disorder. Neuropsychopharmacology. 2013;38:1889–98.CrossRefPubMedPubMedCentral Chen AC, Etkin A. Hippocampal network connectivity and activation differentiates post-traumatic stress disorder from generalized anxiety disorder. Neuropsychopharmacology. 2013;38:1889–98.CrossRefPubMedPubMedCentral
21.
go back to reference Poppenk J, Moscovitch M. A hippocampal marker of recollection memory ability among healthy young adults: contributions of posterior and anterior segments. Neuron. 2011;72:931–7.CrossRefPubMed Poppenk J, Moscovitch M. A hippocampal marker of recollection memory ability among healthy young adults: contributions of posterior and anterior segments. Neuron. 2011;72:931–7.CrossRefPubMed
22.
go back to reference Poppenk J, Evensmoen HR, Moscovitch M, Nadel L. Long-axis specialization of the human hippocampus. Trends Cogn Sci. 2013;17:230–40.CrossRefPubMed Poppenk J, Evensmoen HR, Moscovitch M, Nadel L. Long-axis specialization of the human hippocampus. Trends Cogn Sci. 2013;17:230–40.CrossRefPubMed
23.
go back to reference Chase HW, Clos M, Dibble S, Fox P, Grace AA, Phillips ML, Eickhoff SB. Evidence for an anterior–posterior differentiation in the human hippocampal formation revealed by meta-analytic parcellation of fMRI coordinate maps: focus on the subiculum. NeuroImage. 2015;113:44–60.CrossRefPubMedPubMedCentral Chase HW, Clos M, Dibble S, Fox P, Grace AA, Phillips ML, Eickhoff SB. Evidence for an anterior–posterior differentiation in the human hippocampal formation revealed by meta-analytic parcellation of fMRI coordinate maps: focus on the subiculum. NeuroImage. 2015;113:44–60.CrossRefPubMedPubMedCentral
24.
go back to reference Nadel L, Hoscheidt S, Ryan LR. Spatial cognition and the hippocampus: the anterior–posterior axis. J Cogn Neurosci. 2013;25:22–8.CrossRefPubMed Nadel L, Hoscheidt S, Ryan LR. Spatial cognition and the hippocampus: the anterior–posterior axis. J Cogn Neurosci. 2013;25:22–8.CrossRefPubMed
26.
go back to reference Murty VP, Ritchey M, Adcock RA, LaBar KS. fMRI studies of successful emotional memory encoding: a quantitative meta-analysis. Neuropsychologia. 2010;48:3459–69.CrossRefPubMedPubMedCentral Murty VP, Ritchey M, Adcock RA, LaBar KS. fMRI studies of successful emotional memory encoding: a quantitative meta-analysis. Neuropsychologia. 2010;48:3459–69.CrossRefPubMedPubMedCentral
27.
go back to reference Viard A, Doeller CF, Hartley T, Bird CM, Burgess N. Anterior hippocampus and goal-directed spatial decision making. J Neurosci. 2011;31:4613–21.CrossRefPubMed Viard A, Doeller CF, Hartley T, Bird CM, Burgess N. Anterior hippocampus and goal-directed spatial decision making. J Neurosci. 2011;31:4613–21.CrossRefPubMed
28.
go back to reference Admon R, Milad MR, Hendler T. A causal model of post-traumatic stress disorder: disentangling predisposed from acquired neural abnormalities. Trends Cogn Sci. 2013;17:337–47.CrossRefPubMed Admon R, Milad MR, Hendler T. A causal model of post-traumatic stress disorder: disentangling predisposed from acquired neural abnormalities. Trends Cogn Sci. 2013;17:337–47.CrossRefPubMed
29.
go back to reference Andrews-Hanna JR, Smallwood J, Spreng RN. The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Ann N Y Acad Sci. 2014;1316:29–52.CrossRefPubMedPubMedCentral Andrews-Hanna JR, Smallwood J, Spreng RN. The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Ann N Y Acad Sci. 2014;1316:29–52.CrossRefPubMedPubMedCentral
30.
go back to reference Menon V. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn Sci. 2011;15:483–506.CrossRefPubMed Menon V. Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn Sci. 2011;15:483–506.CrossRefPubMed
31.
go back to reference Lazarov A, Xi Z, Suarez-Jimenez B, Rutherford BR, Neria Y. Resting-state functional connectivity of anterior and posterior hippocampus in posttraumatic stress disorder. J Psychiatr Res. 2017;94:15–22.CrossRefPubMed Lazarov A, Xi Z, Suarez-Jimenez B, Rutherford BR, Neria Y. Resting-state functional connectivity of anterior and posterior hippocampus in posttraumatic stress disorder. J Psychiatr Res. 2017;94:15–22.CrossRefPubMed
32.
go back to reference Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Gusman FD, Charney DS, Keane TM. The development of a clinician-administered PTSD scale. J Trauma Stress. 1995;8:75–90.CrossRefPubMed Blake DD, Weathers FW, Nagy LM, Kaloupek DG, Gusman FD, Charney DS, Keane TM. The development of a clinician-administered PTSD scale. J Trauma Stress. 1995;8:75–90.CrossRefPubMed
33.
go back to reference Lanius RA, Bluhm RL, Coupland NJ, Hegadoren KM, Rowe B, Theberge J, et al. Default mode network connectivity as a predictor of post-traumatic stress disorder symptom severity in acutely traumatized subjects. Acta Psychiatr Scand. 2010;121:33–40.CrossRefPubMed Lanius RA, Bluhm RL, Coupland NJ, Hegadoren KM, Rowe B, Theberge J, et al. Default mode network connectivity as a predictor of post-traumatic stress disorder symptom severity in acutely traumatized subjects. Acta Psychiatr Scand. 2010;121:33–40.CrossRefPubMed
34.
go back to reference Qin L, Wang Z, Sun Y, Wan J, Su S, Zhou Y, Xu J. A preliminary study of alterations in default network connectivity in post-traumatic stress disorder patients following recent trauma. Brain Res. 2012;1484:50–6.CrossRefPubMed Qin L, Wang Z, Sun Y, Wan J, Su S, Zhou Y, Xu J. A preliminary study of alterations in default network connectivity in post-traumatic stress disorder patients following recent trauma. Brain Res. 2012;1484:50–6.CrossRefPubMed
35.
go back to reference Patel R, Girard TA, Pukay-Martin N, Monson C. Preferential recruitment of the basolateral amygdala during memory encoding of negative scenes in posttraumatic stress disorder. Neurobiol Learn Mem. 2016;130:170–6.CrossRefPubMed Patel R, Girard TA, Pukay-Martin N, Monson C. Preferential recruitment of the basolateral amygdala during memory encoding of negative scenes in posttraumatic stress disorder. Neurobiol Learn Mem. 2016;130:170–6.CrossRefPubMed
36.
go back to reference Sheehan DV, Lecrubier Y, Sheehan KH, Janavs J, Weiller E, Keskiner A, et al. The validity of the MINI international neuropsychiatric interview (MINI) according to the SCID-P and its reliability. Eur Psychiatry. 1997;12:232–41.CrossRef Sheehan DV, Lecrubier Y, Sheehan KH, Janavs J, Weiller E, Keskiner A, et al. The validity of the MINI international neuropsychiatric interview (MINI) according to the SCID-P and its reliability. Eur Psychiatry. 1997;12:232–41.CrossRef
37.
go back to reference First MB, Spitzer RL, Gibbon M, Williams JBW. Structured clinical interview for DSM-IV-TR axis I disorders, research version, patient edition with psychotic screen. Biometrics Research: New York; 2002. First MB, Spitzer RL, Gibbon M, Williams JBW. Structured clinical interview for DSM-IV-TR axis I disorders, research version, patient edition with psychotic screen. Biometrics Research: New York; 2002.
38.
go back to reference Beck AT, Steer RA, Brown GK. Beck depression inventory-II. San Antonio. 1996;78:490–8. Beck AT, Steer RA, Brown GK. Beck depression inventory-II. San Antonio. 1996;78:490–8.
39.
go back to reference Yan CG, Wang XD, Zuo XN, Zang YF. DPABI: data processing & analysis for (resting-state) brain imaging. Neuroinformatics. 2016;14:339–51.CrossRefPubMed Yan CG, Wang XD, Zuo XN, Zang YF. DPABI: data processing & analysis for (resting-state) brain imaging. Neuroinformatics. 2016;14:339–51.CrossRefPubMed
40.
go back to reference Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R. Movement-related effects in fMRI time-series. Magn Reson Med. 1996;35:346–55.CrossRefPubMed Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R. Movement-related effects in fMRI time-series. Magn Reson Med. 1996;35:346–55.CrossRefPubMed
41.
go back to reference Behzadi Y, Restom K, Liau J, Liu TT. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage. 2007;37:90–101.CrossRefPubMedPubMedCentral Behzadi Y, Restom K, Liau J, Liu TT. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage. 2007;37:90–101.CrossRefPubMedPubMedCentral
42.
go back to reference Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17:825–41.CrossRefPubMed Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17:825–41.CrossRefPubMed
43.
44.
go back to reference Walter B, Blecker C, Kirsch P, Sammer, G, Schienle A, Stark R, Vaitl D. MARINA: an easy to use tool for the creation of MAsks for region of INterest analyses. Vol. 19. In 9th international conference on functional mapping of the human brain; 2003. Walter B, Blecker C, Kirsch P, Sammer, G, Schienle A, Stark R, Vaitl D. MARINA: an easy to use tool for the creation of MAsks for region of INterest analyses. Vol. 19. In 9th international conference on functional mapping of the human brain; 2003.
45.
go back to reference Shin LM, Rauch SL, Pitman RK. Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Ann N Y Acad Sci. 2006;1071:67–79.CrossRefPubMed Shin LM, Rauch SL, Pitman RK. Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Ann N Y Acad Sci. 2006;1071:67–79.CrossRefPubMed
46.
go back to reference Rorden C, Karnath HO, Bonilha L. Improving lesion-symptom mapping. J Cogn Neurosci. 2007;19:1081–8.CrossRefPubMed Rorden C, Karnath HO, Bonilha L. Improving lesion-symptom mapping. J Cogn Neurosci. 2007;19:1081–8.CrossRefPubMed
47.
go back to reference Boccardi M, Bocchetta M, Apostolova LG, Barnes J, Bartzokis G, Corbetta G, et al. Delphi definition of the EADC-ADNI harmonized protocol for hippocampal segmentation on magnetic resonance. Alzheimers Dement. 2015;11:126–38.CrossRefPubMed Boccardi M, Bocchetta M, Apostolova LG, Barnes J, Bartzokis G, Corbetta G, et al. Delphi definition of the EADC-ADNI harmonized protocol for hippocampal segmentation on magnetic resonance. Alzheimers Dement. 2015;11:126–38.CrossRefPubMed
48.
go back to reference Yehuda R. Status of glucocorticoid alterations in post-traumatic stress disorder. Ann N Y Acad Sci. 2009;1179:56–69.CrossRefPubMed Yehuda R. Status of glucocorticoid alterations in post-traumatic stress disorder. Ann N Y Acad Sci. 2009;1179:56–69.CrossRefPubMed
49.
go back to reference Gurvits TV, Lasko NB, Repak AL, Metzger LJ, Orr SP, Pitman RK. Performance on visuospatial copying tasks in individuals with chronic posttraumatic stress disorder. Psychiatry Res. 2002;112:263–8.CrossRefPubMed Gurvits TV, Lasko NB, Repak AL, Metzger LJ, Orr SP, Pitman RK. Performance on visuospatial copying tasks in individuals with chronic posttraumatic stress disorder. Psychiatry Res. 2002;112:263–8.CrossRefPubMed
50.
go back to reference Tempesta D, Mazza M, Iaria G, De Gennaro L, Ferrara M. A specific deficit in spatial memory acquisition in post-traumatic stress disorder and the role of sleep in its consolidation. Hippocampus. 2012;22:1154–63.CrossRefPubMed Tempesta D, Mazza M, Iaria G, De Gennaro L, Ferrara M. A specific deficit in spatial memory acquisition in post-traumatic stress disorder and the role of sleep in its consolidation. Hippocampus. 2012;22:1154–63.CrossRefPubMed
51.
go back to reference Rabinak CA, Angstadt M, Welsh RC, Kenndy AE, Lyubkin M, Martis B, Phan KL. Altered amygdala resting-state functional connectivity in post-traumatic stress disorder. Front Psychiatry. 2011;2:1–8.CrossRef Rabinak CA, Angstadt M, Welsh RC, Kenndy AE, Lyubkin M, Martis B, Phan KL. Altered amygdala resting-state functional connectivity in post-traumatic stress disorder. Front Psychiatry. 2011;2:1–8.CrossRef
52.
go back to reference Button KS, Ioannidis JP, Mokrysz C, Nosek BA, Flint J, Robinson ES, et al. Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci. 2013;14:365–76.CrossRefPubMed Button KS, Ioannidis JP, Mokrysz C, Nosek BA, Flint J, Robinson ES, et al. Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci. 2013;14:365–76.CrossRefPubMed
53.
go back to reference Munafò MR, Nosek BA, Bishop DV, Button KS, Chambers CD, du Sert NP, et al. A manifesto for reproducible science. Nat Hum Behav. 2017;1:21.CrossRef Munafò MR, Nosek BA, Bishop DV, Button KS, Chambers CD, du Sert NP, et al. A manifesto for reproducible science. Nat Hum Behav. 2017;1:21.CrossRef
54.
go back to reference Birn RM, Molloy EK, Patriat R, Parker T, Meier TB, Kirk GR, et al. The effect of scan length on the reliability of resting-state fMRI connectivity estimates. NeuroImage. 2013;83:550–8.CrossRefPubMedPubMedCentral Birn RM, Molloy EK, Patriat R, Parker T, Meier TB, Kirk GR, et al. The effect of scan length on the reliability of resting-state fMRI connectivity estimates. NeuroImage. 2013;83:550–8.CrossRefPubMedPubMedCentral
55.
56.
go back to reference Nicholson AA, Densmore M, Frewen PA, Theberge J, Neufeld RWJ, McKinnon MC, Lanius RA. The dissociative subtype of posttramatic stress disorder: unique resting-state functional connectivity of basolateral and centromedial amygdala complexes. Neuropsychopharmacology. 2015;40:2317–26.CrossRefPubMedPubMedCentral Nicholson AA, Densmore M, Frewen PA, Theberge J, Neufeld RWJ, McKinnon MC, Lanius RA. The dissociative subtype of posttramatic stress disorder: unique resting-state functional connectivity of basolateral and centromedial amygdala complexes. Neuropsychopharmacology. 2015;40:2317–26.CrossRefPubMedPubMedCentral
Metadata
Title
Functional connectivity of hippocampal subregions in PTSD: relations with symptoms
Authors
Bailee L. Malivoire
Todd A. Girard
Ronak Patel
Candice M. Monson
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Psychiatry / Issue 1/2018
Electronic ISSN: 1471-244X
DOI
https://doi.org/10.1186/s12888-018-1716-9

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