Manual segmentation of the paraventricular nucleus of the hypothalamus and the dorsal and ventral bed nucleus of stria terminalis using multimodal 7 Tesla structural MRI: probabilistic atlases for a stress-control triad.
Anxiety
Bed nucleus of stria terminalis
Manual segmentation
Paraventricular nucleus of hypothalamus
Probabilistic atlas
Stress
Journal
Brain structure & function
ISSN: 1863-2661
Titre abrégé: Brain Struct Funct
Pays: Germany
ID NLM: 101282001
Informations de publication
Date de publication:
09 Oct 2023
09 Oct 2023
Historique:
received:
29
01
2023
accepted:
18
09
2023
medline:
9
10
2023
pubmed:
9
10
2023
entrez:
9
10
2023
Statut:
aheadofprint
Résumé
The paraventricular nucleus of the hypothalamus (PVN) is uniquely capable of proximal control over autonomic and neuroendocrine stress responses, and the bed nucleus of the stria terminalis (BNST) directly modulates PVN function, as well as playing an important role in stress control itself. The dorsal BNST (dBNST) is predominantly preautonomic, while the ventral BNST (vBNST) is predominantly viscerosensory, receiving dense noradrenergic signaling. Distinguishing the dBNST and vBNST, along with the PVN, may facilitate our understanding of dynamic interactions among these regions. T1-weighted MPRAGE and high resolution gradient echo (GRE) modalities were acquired at 7T. GRE was coregistered to MPRAGE and segmentations were performed in MRIcroGL based on their Atlas of the Human Brain depictions. The dBNST, vBNST and PVN were manually segmented in 25 participants; 10 images were rated by 2 raters. These segmentations were normalized and probabilistic atlases for each region were generated in MNI space, now available as resources for future research. We found moderate-high inter-rater reliability [n = 10; Mean Dice (SD); PVN = 0.69 (0.04); dBNST = 0.77 (0.04); vBNST = 0.62 (0.04)]. Probabilistic atlases were reverse normalized into native space for six additional participants that were segmented but not included in the original 25. We also found moderate to moderate-high reliability between the probabilistic atlases and manual segmentations [n = 6; Mean Dice (SD); PVN = 0.55 (0.12); dBNST = 0.60 (0.10); vBNST = 0.47 (0.12 SD)]. By isolating these hypothalamic and BNST subregions using ultra-high field MRI modalities, more specific delineations of these regions can facilitate greater understanding of mechanisms underlying stress-related function and psychopathology.
Identifiants
pubmed: 37812278
doi: 10.1007/s00429-023-02713-z
pii: 10.1007/s00429-023-02713-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIMH NIH HHS
ID : R01 MH120065
Pays : United States
Informations de copyright
© 2023. The Author(s).
Références
Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26(3):839–851
doi: 10.1016/j.neuroimage.2005.02.018
pubmed: 15955494
Aston-Jones G, Delfs JM, Druhan J, Zhu Y (1999) The bed nucleus of the stria terminalis: a target site for noradrenergic actions in opiate withdrawal. Ann N Y Acad Sci 877:486–498
doi: 10.1111/j.1749-6632.1999.tb09284.x
pubmed: 10415666
Avery SN, Clauss JA, Winder DG, Woodward N, Heckers S, Blackford JU (2014) BNST neurocircuitry in humans. Neuroimage 91:311–323. https://doi.org/10.1016/j.neuroimage.2014.01.017
doi: 10.1016/j.neuroimage.2014.01.017
pubmed: 24444996
Avery SN, Clauss JA, Blackford JU (2016) The human BNST: functional role in anxiety and addiction. Neuropsychopharmacology 41(1):126–141. https://doi.org/10.1038/npp.2015.185
doi: 10.1038/npp.2015.185
pubmed: 26105138
Banihashemi L, Rinaman L (2006) Noradrenergic inputs to the bed nucleus of the stria terminalis and paraventricular nucleus of the hypothalamus underlie hypothalamic-pituitary-adrenal axis but not hypophagic or conditioned avoidance responses to systemic yohimbine. J Neurosci 26(44):11442–11453
doi: 10.1523/JNEUROSCI.3561-06.2006
pubmed: 17079674
pmcid: 6674526
Banihashemi L, Rinaman L (2010) Repeated brief postnatal maternal separation enhances hypothalamic gastric autonomic circuits in juvenile rats. Neuroscience 165(1):265–277
doi: 10.1016/j.neuroscience.2009.09.081
pubmed: 19800939
Banihashemi L, O’Neill EJ, Rinaman L (2011) Central neural responses to restraint stress are altered in rats with an early life history of repeated brief maternal separation. Neuroscience 192:413–428. https://doi.org/10.1016/j.neuroscience.2011.06.052
doi: 10.1016/j.neuroscience.2011.06.052
pubmed: 21736922
Banihashemi L, Sheu LK, Midei AJ, Gianaros PJ (2015) Childhood physical abuse predicts stressor-evoked activity within central visceral control regions. Soc Cogn Affect Neurosci 10(4):474–485. https://doi.org/10.1093/scan/nsu073
doi: 10.1093/scan/nsu073
pubmed: 24847113
Banihashemi L, Peng CW, Rangarajan A, Karim HT, Wallace ML, Sibbach BM, Singh J, Stinley MM, Germain A, Aizenstein HJ (2022) Childhood threat is associated with lower resting-state connectivity within a central visceral network. Front Psychol. https://doi.org/10.3389/fpsyg.2022.805049
doi: 10.3389/fpsyg.2022.805049
pubmed: 35310241
pmcid: 8927539
Billot B, Bocchetta M, Todd E, Dalca AV, Rohrer JD, Iglesias JE (2020) Automated segmentation of the hypothalamus and associated subunits in brain MRI. Neuroimage 223:117287. https://doi.org/10.1016/j.neuroimage.2020.117287PMID-32853816
doi: 10.1016/j.neuroimage.2020.117287PMID-32853816
pubmed: 32853816
Card JP, Levitt P, Gluhovsky M, Rinaman L (2005) Early experience modifies the postnatal assembly of autonomic emotional motor circuits in rats. J Neurosci 25(40):9102–9111
doi: 10.1523/JNEUROSCI.2345-05.2005
pubmed: 16207869
pmcid: 6725770
Cecchi M, Khoshbouei H, Javors M, Morilak DA (2002) Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress. Neuroscience 112(1):13–21
doi: 10.1016/S0306-4522(02)00062-3
pubmed: 12044468
Charney DS (2003) The psychobiology of resilience and vulnerability to anxiety disorders: implications for prevention and treatment. Dialogues Clin Neurosci 5(3):207–221
Choi DC, Dolgas CM, Herman JP (2004) The role of the bed nucleus of the stria terminalis in regulating the HPA axis. Paper presented at the Society for Neuroscience, Washington, DC
Choi DC, Evanson NK, Furay AR, Ulrich-Lai YM, Ostrander MM, Herman JP (2007a) The anteroventral bed nucleus of the stria terminalis differentially regulates hypothalamic-pituitary-adrenocortical axis responses to acute and chronic stress. Endocrinology 149(2):818–826. https://doi.org/10.1210/en.2007-0883
doi: 10.1210/en.2007-0883
pubmed: 18039788
pmcid: 2219312
Choi DC, Furay AR, Evanson NK, Ostrander MM, Ulrich-Lai YM, Herman JP (2007b) Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs. J Neurosci 27(8):2025–2034
doi: 10.1523/JNEUROSCI.4301-06.2007
pubmed: 17314298
pmcid: 6673539
Crestani CC, Alves FHF, Gomes FV, Resstel LBM, Correa FMA, Herman JP (2013) Mechanisms in the bed nucleus of the stria terminalis involved in control of autonomic and neuroendocrine functions: a review. Curr Neuropharmacol 11(2):141–159. https://doi.org/10.2174/1570159x11311020002PMID-23997750
doi: 10.2174/1570159x11311020002PMID-23997750
pubmed: 23997750
pmcid: 3637669
Cullinan WE, Herman JP (1993) Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of the stria terminalis. J Comp Neurol 332(1):1–20
doi: 10.1002/cne.903320102
pubmed: 7685778
Davis M, Walker DL, Miles L, Grillon C (2010) Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 35(1):105–135
doi: 10.1038/npp.2009.109
pubmed: 19693004
Delfs J, Zhu Y, Druhan JP, Aston-Jones G (2000) Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion. Nature 403(27):430–434
doi: 10.1038/35000212
pubmed: 10667795
Dong H-W, Swanson LW (2003) Projections from the rhomboid nucleus of the bed nuclei of the stria terminalis: implications for cerebral hemisphere regulation of ingestive behaviors. J Comp Neurol 463:434–472
doi: 10.1002/cne.10758
pubmed: 12836178
Dong H-W, Swanson LW (2004) Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis. J Comp Neurol 468:277–298
doi: 10.1002/cne.10949
pubmed: 14648685
Dong H-W, Petrovich GD, Watts AG, Swanson LW (2001) Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain. J Comp Neurol 436:430–455
doi: 10.1002/cne.1079
pubmed: 11447588
Elin K, Malyutina S, Bronov O, Stupina E, Marinets A, Zhuravleva A, Dragoy O (2022) A new functional magnetic resonance imaging localizer for preoperative language mapping using a sentence completion task: validity, choice of baseline condition, and test–retest reliability. Front Human Neurosci 16:791577
Fendt M, Endres T, Apfelbach R (2003T) emporary inactivation of the bed nucleus of the stria terminalis but not of the amygdala blocks freezing induced by trimethylthiazoline, a component of fox feces. J Neurosci 23(1):23–28
doi: 10.1523/JNEUROSCI.23-01-00023.2003
pubmed: 12514197
pmcid: 6742150
Fendt M, Siegl S, Steiniger-Brach B (2005) Noradrenaline transmission within the ventral bed nucleus of the stria terminalis is critical for fear behavior induced by trimethylthiazoline, a component of fox odor. J Neurosci 25(25):5998–6004
doi: 10.1523/JNEUROSCI.1028-05.2005
pubmed: 15976089
pmcid: 6724787
Flook EA, Feola B, Benningfield MM, Silveri MM, Winder DG, Blackford JU (2021) Alterations in connectivity of the bed nucleus of the stria terminalis during early abstinence in individuals with alcohol use disorder. Alcohol Clin Exp Res 45(5):1028–1038. https://doi.org/10.1111/acer.14596PMID-33830508
doi: 10.1111/acer.14596PMID-33830508
pubmed: 33830508
Fox AS, Shelton SE, Oakes TR, Davidson RJ, Kalin NH (2008) Trait-like brain activity during adolescence predicts anxious temperament in primates. PLoS ONE 3(7):e2570. https://doi.org/10.1371/journal.pone.0002570.t002
doi: 10.1371/journal.pone.0002570.t002
pubmed: 18596957
pmcid: 2430534
Fox AS, Oler JA, Birn RM, Shackman AJ, Alexander AL, Kalin NH (2018) Functional connectivity within the primate extended amygdala is heritable and associated with early-life anxious temperament. J Neurosci 38(35):7611–7621. https://doi.org/10.1523/jneurosci.0102-18.2018PMID-30061190
doi: 10.1523/jneurosci.0102-18.2018PMID-30061190
pubmed: 30061190
pmcid: 6113902
Goldstein RB, Smith SM, Chou SP, Saha TD, Jung J, Zhang H, Pickering RP, Ruan WJ, Huang B, Grant BF (2016) The epidemiology of DSM-5 posttraumatic stress disorder in the United States: results from the National Epidemiologic Survey on Alcohol and Related Conditions-III. Soc Psychiatry Psychiatr Epidemiol 51:1137–1148
doi: 10.1007/s00127-016-1208-5
pubmed: 27106853
pmcid: 4980174
Gray TS, Piechowski RA (1993) Ibotenic acid lesions of the bed nucleus of the stria terminalis attenuate conditioned stress-induced increases in prolactin, ACTH and corticosterone. Neuroendocrinology 57:517–524
doi: 10.1159/000126400
pubmed: 8391664
Hart H, Rubia K (2012) Neuroimaging of child abuse: a critical review. Front Hum Neurosci 6:52
doi: 10.3389/fnhum.2012.00052
pubmed: 22457645
pmcid: 3307045
Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20(2):78–84
doi: 10.1016/S0166-2236(96)10069-2
pubmed: 9023876
Herman JP, Tasker JG (2016) Paraventricular hypothalamic mechanisms of chronic stress adaptation. Front Endocrinol 7:137
doi: 10.3389/fendo.2016.00137
Herman JP, Cullinan WE, Watson SJ (1994) Involvement of the bed nucleus of the stria terminalis in tonic regulation of paraventricular hypothalamic CRH and AVP mRNA expression. J Neuroendocrinol 6(4):433–442
doi: 10.1111/j.1365-2826.1994.tb00604.x
pubmed: 7987374
Herman JP, Cullinan WE, Ziegler DR, Tasker JG (2002) Role of the paraventricular nucleus microenvironment in stress integration. Eur J Neurosci 16(3):381–385
doi: 10.1046/j.1460-9568.2002.02133.x
pubmed: 12193178
Johnson SB, Emmons EB, Anderson RM, Glanz RM, Romig-Martin SA, Narayanan NS, LaLumiere RT, Radley JJ (2016) A basal forebrain site coordinates the modulation of endocrine and behavioral stress responses via divergent neural pathways. J Neurosci 36(33):8687–8699. https://doi.org/10.1523/jneurosci.1185-16.2016PMID-27535914
doi: 10.1523/jneurosci.1185-16.2016PMID-27535914
pubmed: 27535914
pmcid: 4987438
Kessler RC, Petukhova M, Sampson NA, Zaslavsky AM, Wittchen HU (2012) Twelve-month and lifetime prevalence and lifetime morbid risk of anxiety and mood disorders in the United States. Int J Methods Psychiatr Res 21(3):169–184
doi: 10.1002/mpr.1359
pubmed: 22865617
pmcid: 4005415
Koenen KC, Ratanatharathorn A, Ng L, McLaughlin KA, Bromet EJ, Stein DJ, Karam EG, Ruscio AM, Benjet C, Scott K (2017) Posttraumatic stress disorder in the world mental health surveys. Psychol Med 47(13):2260–2274
doi: 10.1017/S0033291717000708
pubmed: 28385165
pmcid: 6034513
Krishnamurthy N, Santini T, Wood S, Kim J, Zhao T, Aizenstein HJ, Ibrahim TS (2019) Computational and experimental evaluation of the Tic-Tac-Toe RF coil for 7Tesla MRI. PLoS ONE 14(1):e0209663. https://doi.org/10.1371/journal.pone.0209663
doi: 10.1371/journal.pone.0209663
pubmed: 30629618
pmcid: 6328242
Leri F, Flores J, Rodaros D, Stewart J (2002) Blockade of stress-induced but not cocaine-induced reinstatement by infusion of noradrenergic antagonists into the bed nucleus of the stria terminalis or the central nucleus of the amygdala. J Neurosci 22(13):5713–5718
doi: 10.1523/JNEUROSCI.22-13-05713.2002
pubmed: 12097523
pmcid: 6758192
Levine S (1971) Stress and behavior. Sci Am 224(1):26–31
doi: 10.1038/scientificamerican0171-26
pubmed: 4992286
Luiten PGM, Ter Horst GJ, Karst H, Steffens AB (1985) The course of paraventricular hypothalamic efferents to autonomic structures in medulla and spinal cord. Brain Res 329(1–2):374–378
doi: 10.1016/0006-8993(85)90554-2
pubmed: 3978460
Mai JK, Paxinos G, Voss T (2008) Atlas of the human brain, 3rd edn. Academic Press, New York
Maita I, Bazer A, Blackford JU, Samuels BA (2021) Chapter 27 Functional anatomy of the bed nucleus of the stria terminalis–hypothalamus neural circuitry: Implications for valence surveillance, addiction, feeding, and social behaviors. Handb Clin Neurol 179:403–418. https://doi.org/10.1016/b978-0-12-819975-6.00026-1PMID-34225978
doi: 10.1016/b978-0-12-819975-6.00026-1PMID-34225978
pubmed: 34225978
Makris N, Swaab DF, Avd K, Abbs B, Boriel D, Handa RJ, Tobet S, Goldstein JM (2013) Volumetric parcellation methodology of the human hypothalamus in neuroimaging: normative data and sex differences. Neuroimage 69:1–10. https://doi.org/10.1016/j.neuroimage.2012.12.008PMID-23247186
doi: 10.1016/j.neuroimage.2012.12.008PMID-23247186
pubmed: 23247186
Neudorfer C, Germann J, Elias GJB, Gramer R, Boutet A, Lozano AM (2020) A high-resolution in vivo magnetic resonance imaging atlas of the human hypothalamic region. Sci Data 7(1):305. https://doi.org/10.1038/s41597-020-00644-6PMID-32934244
doi: 10.1038/s41597-020-00644-6PMID-32934244
pubmed: 32934244
pmcid: 7492465
Penny WD, Friston KJ, Ashburner JT, Kiebel SJ, Nichols TE (2011) Statistical parametric mapping: the analysis of functional brain images. Elsevier
Radley JJ, Johnson SB (2018) Anteroventral bed nuclei of the stria terminalis neurocircuitry: towards an integration of HPA axis modulation with coping behaviors—Curt Richter Award Paper 2017. Psychoneuroendocrinology 89:239–249. https://doi.org/10.1016/j.psyneuen.2017.12.005PMID-29395488
doi: 10.1016/j.psyneuen.2017.12.005PMID-29395488
pubmed: 29395488
Radley JJ, Gosselink KL, Sawchenko PE (2009) A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuroendocrine stress response. J Neurosci 29(22):7330–7340. https://doi.org/10.1523/jneurosci.5924-08.2009
doi: 10.1523/jneurosci.5924-08.2009
pubmed: 19494154
pmcid: 2743123
Reul J, Kloet ERd (1985) Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117(6):2505–2511
doi: 10.1210/endo-117-6-2505
pubmed: 2998738
Riche D, DePommery J (1990) Neuropeptides and catecholamines in efferent projections of the nuclei of the solitary tract in the rat. J Comp Neurol 293:399–424
doi: 10.1002/cne.902930306
pubmed: 1969868
Rinaman L, Banihashemi L, Koehnle TJ (2011) Early life experience shapes the functional organization of stress-responsive visceral circuits. Physiol Behav 104(4):632–640
doi: 10.1016/j.physbeh.2011.04.008
Santini T, Kim J, Wood S, Krishnamurthy N, Farhat N, Maciel C, Raval SB, Zhao T, Ibrahim TS (2018a) A new RF transmit coil for foot and ankle imaging at 7T MRI. Magn Reson Imaging 45:1–6. https://doi.org/10.1016/j.mri.2017.09.005
doi: 10.1016/j.mri.2017.09.005
pubmed: 28893660
Santini T, Zhao Y, Wood S, Krishnamurthy N, Kim J, Farhat N, Alkhateeb S, Martins T, Koo M, Zhao T, Aizenstein HJ, Ibrahim TS (2018b) In-vivo and numerical analysis of the eigenmodes produced by a multi-level Tic-Tac-Toe head transmit array for 7Tesla MRI. PLoS ONE 13(11):e0206127. https://doi.org/10.1371/journal.pone.0206127
doi: 10.1371/journal.pone.0206127
pubmed: 30481187
pmcid: 6258503
Santini T, Wood S, Krishnamurthy N, Martins T, Aizenstein HJ, Ibrahim TS (2021) Improved 7Tesla transmit field homogeneity with reduced electromagnetic power deposition using coupled Tic Tac Toe antennas. Sci Rep 11(1):3370. https://doi.org/10.1038/s41598-020-79807-9
doi: 10.1038/s41598-020-79807-9
pubmed: 33564013
pmcid: 7873125
Schindler S, Schönknecht P, Schmidt L, Anwander A, Strauß M, Trampel R, Bazin P-L, Möller HE, Hegerl U, Turner R, Geyer S (2013) Development and evaluation of an algorithm for the computer-assisted segmentation of the human hypothalamus on 7-Tesla magnetic resonance images. PLoS ONE 8(7):e66394. https://doi.org/10.1371/journal.pone.0066394PMID-23935821
doi: 10.1371/journal.pone.0066394PMID-23935821
pubmed: 23935821
pmcid: 3720799
Schweimer J, Fendt M, Schnitzler H-U (2005) Effects of clonidine injections into the bed nucleus of the stria terminalis on fear and anxiety behavior in rats. Eur J Pharmacol 507:117–124
doi: 10.1016/j.ejphar.2004.11.044
pubmed: 15659301
Shackman AJ, Fox AS, Oler JA, Shelton SE, Oakes TR, Davidson RJ, Kalin NH (2017) Heightened extended amygdala metabolism following threat characterizes the early phenotypic risk to develop anxiety-related psychopathology. Mol Psychiatry 22(5):724–732. https://doi.org/10.1038/mp.2016.132PMID-27573879
doi: 10.1038/mp.2016.132PMID-27573879
pubmed: 27573879
Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (MINI): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59(20):22–33
pubmed: 9881538
Sink KS, Davis M, Walker DL (2013) CGRP antagonist infused into the bed nucleus of the stria terminalis impairs the acquisition and expression of context but not discretely cued fear. Learn Mem 20(12):730–739
doi: 10.1101/lm.032482.113
pubmed: 24255102
pmcid: 3834624
Spindler M, Özyurt J, Thiel CM (2020) Automated diffusion-based parcellation of the hypothalamus reveals subunit-specific associations with obesity. Sci Rep 10(1):22238. https://doi.org/10.1038/s41598-020-79289-9PMID-33335266
doi: 10.1038/s41598-020-79289-9PMID-33335266
pubmed: 33335266
pmcid: 7747731
Sullivan GM, Apergis J, Bush DEA, Johnson LR, Hou M, Ledoux JE (2004) Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus. Neuroscience 128:7–14
doi: 10.1016/j.neuroscience.2004.06.015
pubmed: 15450349
Theiss JD, Ridgewell C, McHugo M, Heckers S, Blackford JU (2017) Manual segmentation of the human bed nucleus of the stria terminalis using 3T MRI. Neuroimage 146(C):288–292. https://doi.org/10.1016/j.neuroimage.2016.11.047
doi: 10.1016/j.neuroimage.2016.11.047
pubmed: 27876653
Torrisi S, O’Connell K, Davis A, Reynolds R, Balderston N, Fudge JL, Grillon C, Ernst M (2015) Resting state connectivity of the bed nucleus of the stria terminalis at ultra-high field. Hum Brain Mapp 36(10):4076–4088. https://doi.org/10.1002/hbm.22899PMID-26178381
doi: 10.1002/hbm.22899PMID-26178381
pubmed: 26178381
pmcid: 4583367
Walker DL, Davis M (1997) Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17(23):9375–9383
doi: 10.1523/JNEUROSCI.17-23-09375.1997
pubmed: 9364083
pmcid: 6573581
Wilson SM, Bautista A, Yen M, Lauderdale S, Eriksson DK (2017) Validity and reliability of four language mapping paradigms. NeuroImage Clin 16:399–408. https://doi.org/10.1016/j.nicl.2016.03.015
doi: 10.1016/j.nicl.2016.03.015
pubmed: 28879081
Wolff J, Schindler S, Lucas C, Binninger A-S, Weinrich L, Schreiber J, Hegerl U, Möller HE, Leitzke M, Geyer S, Schönknecht P (2018) A semi-automated algorithm for hypothalamus volumetry in 3Tesla magnetic resonance images. Psychiatry Res Neuroimaging 277:45–51. https://doi.org/10.1016/j.pscychresns.2018.04.007PMID-29776867
doi: 10.1016/j.pscychresns.2018.04.007PMID-29776867
pubmed: 29776867
Wu M, Mennin DS, Ly M, Karim HT, Banihashemi L, Tudorascu DL, Aizenstein HJ, Andreescu C (2019) When worry may be good for you: Worry severity and limbic-prefrontal functional connectivity in late-life generalized anxiety disorder. J Affect Disord 257:650–657. https://doi.org/10.1016/j.jad.2019.07.022
doi: 10.1016/j.jad.2019.07.022
pubmed: 31357162
pmcid: 6711791