Advertisement

Changes in brain glucose metabolism and connectivity in somatoform disorders: an 18F-FDG PET study

  • Qi Huang
  • Shuhua Ren
  • Donglang Jiang
  • Yihui Guan
  • Fang XieEmail author
  • Daliang SunEmail author
  • Fengchun HuaEmail author
Original Paper
  • 33 Downloads

Abstract

Somatoform disorders (SFD) are defined as a syndrome characterized by somatic symptoms which cannot be explained by organic reasons. Chronic or recurrent forms of somatization lead to heavy emotional and financial burden to the patients and their families. However, the underlying etiology of SFD is largely unknown. The purpose of this study is to investigate the changed brain glucose metabolic pattern in SFD. In this study, 18 SFD patients and 21 matched healthy controls were enrolled and underwent an 18F-FDG PET scan. First, we explored the altered brain glucose metabolism in SFD. Then, we calculated the mean 18F-FDG uptake values for 90 AAL regions, and detected the changed brain metabolic connectivity between the most significantly changed regions and all other regions. In addition, the Pearson coefficients between the neuropsychological scores and regional brain 18F-FDG uptake values were computed for SFD patients. We found that SFD patients showed extensive hypometabolism in bilateral superolateral prefrontal cortex, insula, and regions in bilateral temporal gyrus, right angular gyrus, left gyrus rectus, right fusiform gyrus, right rolandic operculum and bilateral occipital gyrus. The metabolic connectivity between right insula and prefrontal areas, as well as within prefrontal areas was enhanced in SFD. And several brain regions were associated with the somatic symptoms, including insula, putamen, middle temporal gyrus, superior parietal gyrus and orbital part of inferior frontal gyrus. Our study revealed widespread alterations of the brain glucose metabolic pattern in SFD patients. Those findings might elucidate the neuronal mechanisms with glucose metabolism and shed light on the pathology of SFD.

Keywords

Somatoform disorders 18F-FDG PET Brain connectivity Insula Prefrontal cortex 

Notes

Compliance with ethical standards

Conflict of interest

All authors declare no conflict of interest regarding the present study. This study was sponsored by the Shanghai Sailing Program (19YF1405300), startup fund of Huashan Hospital, Fudan University (837) to QH; the National Science Foundation of China (81801752), Shanghai Sailing Program (18YF1403200) and startup fund of Huashan Hospital, Fudan University (2017QD081) to XF; Science and Technology Commission of Shanghai Municipality (Grant number 17411953500) to YG; and Key project of the Tianjin Health and Family Planning Commission (2015KR01) to DS.

Ethical standards

All the participants or their guardians provided informed consent prior to their inclusion in the study. This study and was approved by the institutional review boards of Huashan hospital, Fudan University, and was conducted following Declaration of Helsinki guidelines.

Supplementary material

406_2019_1083_MOESM1_ESM.docx (1.3 mb)
Supplementary file1 (DOCX 1301 kb)

References

  1. 1.
    Wittchen HU, Jacobi F, Rehm J, Gustavsson A, Svensson M, Jonsson B, Olesen J, Allgulander C, Alonso J, Faravelli C, Fratiglioni L, Jennum P, Lieb R, Maercker A, van Os J, Preisig M, Salvador-Carulla L, Simon R, Steinhausen HC (2011) The size and burden of mental disorders and other disorders of the brain in Europe 2010. Eur Neuropsychopharmacol 21(9):655–679.  https://doi.org/10.1016/j.euroneuro.2011.07.018 PubMedGoogle Scholar
  2. 2.
    Sartorius N, Ustun TB, Lecrubier Y, Wittchen HU (1996) Depression comorbid with anxiety: results from the WHO study on psychological disorders in primary health care. Br J Psychiatry 168:38–43.  https://doi.org/10.1192/s0007125000298395 Google Scholar
  3. 3.
    Baumeister H, Harter M (2007) Prevalence of mental disorders based on general population surveys. Soc Psychiatry Psychiatr Epidemiol 42(7):537–546.  https://doi.org/10.1007/s00127-007-0204-1 PubMedGoogle Scholar
  4. 4.
    Boeckle M, Schrimpf M, Liegl G, Pieh C (2016) Neural correlates of somatoform disorders from a meta-analytic perspective on neuroimaging studies. Neuroimage Clin 11(C):606–613PubMedPubMedCentralGoogle Scholar
  5. 5.
    Barsky AJ, Orav EJ, Bates DW (2005) Somatization increases medical utilization and costs independent of psychiatric and medical comorbidity. Arch Gen Psychiatry 62(8):903–910.  https://doi.org/10.1001/archpsyc.62.8.903 PubMedGoogle Scholar
  6. 6.
    Gustavsson A, Svensson M, Jacobi F, Allgulander C, Alonso J, Beghi E, Dodel R, Ekman M, Faravelli C, Fratiglioni L, Gannon B, Jones DH, Jennum P, Jordanova A, Jonsson L, Karampampa K, Knapp M, Kobelt G, Kurth T, Lieb R, Linde M, Ljungcrantz C, Maercker A, Melin B, Moscarelli M, Musayev A, Norwood F, Preisig M, Pugliatti M, Rehm J, Salvador-Carulla L, Schlehofer B, Simon R, Steinhausen HC, Stovner LJ, Vallat JM, Van den Bergh P, van Os J, Vos P, Xu WL, Wittchen HU, Jonsson B, Olesen J, Grp CS (2011) Cost of disorders of the brain in Europe 2010. Eur Neuropsychopharmacol 21(10):718–779.  https://doi.org/10.1016/j.euroneuro.2011.08.008 PubMedGoogle Scholar
  7. 7.
    Olesen J, Gustavsson A, Svensson M, Wittchen HU, Jonsson B, Grp CS, European Brain C (2012) The economic cost of brain disorders in Europe. Eur J Neurol 19(1):155–162.  https://doi.org/10.1111/j.1468-1331.2011.03590.x PubMedGoogle Scholar
  8. 8.
    Yildirim H, Atmaca M, Sirlier B, Kayali A (2012) Pituitary volumes are reduced in patients with somatization disorder. Psychiatry Investig 9(3):278–282.  https://doi.org/10.4306/pi.2012.9.3.278 PubMedPubMedCentralGoogle Scholar
  9. 9.
    Atmaca M, Sirlier B, Yildirim H, Kayali A (2011) Hippocampus and amygdalar volumes in patients with somatization disorder. Prog Neuropsychopharmacol Biol Psychiatry 35(7):1699–1703.  https://doi.org/10.1016/j.pnpbp.2011.05.016 PubMedGoogle Scholar
  10. 10.
    Atmaca M, Baykara S, Mermi O, Yildirim H, Akaslan U (2015) Pituitary volumes are changed in patients with conversion disorder. Brain Imaging Behav 10(1):1–4Google Scholar
  11. 11.
    Hakala M, Karlsson H, Kurki T, Aalto S, Koponen S, Vahlberg T, Niemi PM (2004) Volumes of the caudate nuclei in women with somatization disorder and healthy women. Psychiatry Res 131(1):71–78PubMedGoogle Scholar
  12. 12.
    Perez DL, Matin N, Williams B, Tanev K, Makris N, LaFrance WC Jr, Dickerson BC (2018) Cortical thickness alterations linked to somatoform and psychological dissociation in functional neurological disorders. Hum Brain Mapp 39(1):428–439.  https://doi.org/10.1002/hbm.23853 PubMedGoogle Scholar
  13. 13.
    Hakala M, Vahlberg T, Niemi PM, Karlsson H (2006) Brain glucose metabolism and temperament in relation to severe somatization. Psychiatry Clin Neurosci 60(6):669–675.  https://doi.org/10.1111/j.1440-1819.2006.01581.x PubMedGoogle Scholar
  14. 14.
    Hakala M, Karlsson H, Ruotsalainen U, Koponen S, Bergman J, Stenman H, Kelavuori JP, Aalto S, Kurki T, Niemi P (2002) Severe somatization in women is associated with altered cerebral glucose metabolism. Psychol Med 32(8):1379–1385.  https://doi.org/10.1017/s0033291702006578 PubMedGoogle Scholar
  15. 15.
    Horwitz B, Duara R, Rapoport SI (1984) Intercorrelations of glucose metabolic rates between brain regions: application to healthy males in a state of reduced sensory input. J Cerebr Blood Flow Metab 4(4):484Google Scholar
  16. 16.
    Hu Y, Xu Q, Li K, Zhu H, Qi R, Zhang Z, Lu G (2013) Gender differences of brain glucose metabolic networks revealed by FDG-PET: evidence from a large cohort of 400 young adults. PLoS O ne 8(12):e83821.  https://doi.org/10.1371/journal.pone.0083821 Google Scholar
  17. 17.
    Choi H, Choi Y, Kim KW, Kang H, Kim EE, Chung J-K, Lee DS (2015) Maturation of metabolic connectivity of the adolescent rat brain. Elife 4:e11571PubMedPubMedCentralGoogle Scholar
  18. 18.
    Huang Q, Zhang J, Zhang T, Wang H, Yan J (2019) Age-associated reorganization of metabolic brain connectivity in Chinese children. Eur J Nucl Med Mol Imaging.  https://doi.org/10.1007/s00259-019-04508-z PubMedPubMedCentralGoogle Scholar
  19. 19.
    Morbelli S, Drzezga A, Perneczky R, Frisoni GB, Caroli A, van Berckel BN, Ossenkoppele R, Guedj E, Didic M, Brugnolo A (2012) Resting metabolic connectivity in prodromal Alzheimer's disease. A European Alzheimer Disease Consortium (EADC) project. Neurobiol Aging 33(11):2533–2550PubMedGoogle Scholar
  20. 20.
    Perani D, Farsad M, Ballarini T, Lubian F, Malpetti M, Fracchetti A, Magnani G, March A, Abutalebi J (2017) The impact of bilingualism on brain reserve and metabolic connectivity in Alzheimer's dementia. Proc Natl Acad Sci 114(7):1690–1695.  https://doi.org/10.1073/pnas.1610909114 PubMedGoogle Scholar
  21. 21.
    Ballarini T, Iaccarino L, Magnani G, Ayakta N, Miller BL, Jagust WJ, Gorno-Tempini ML, Rabinovici GD, Perani D (2016) Neuropsychiatric subsyndromes and brain metabolic network dysfunctions in early onset Alzheimer's disease. Hum Brain Mapp 37(12):4234–4247PubMedGoogle Scholar
  22. 22.
    Im H-J, Hahm J, Kang H, Choi H, Lee H, Kim EE, Chung J-K, Lee DS (2016) Disrupted brain metabolic connectivity in a 6-OHDA-induced mouse model of Parkinson’s disease examined using persistent homology-based analysis. Scientific reports 6:33875PubMedPubMedCentralGoogle Scholar
  23. 23.
    Sala A, Caminiti SP, Presotto L, Premi E, Pilotto A, Turrone R, Cosseddu M, Alberici A, Paghera B, Borroni B, Padovani A, Perani D (2017) Altered brain metabolic connectivity at multiscale level in early Parkinson’s disease. Sci Rep 7(1):4256.  https://doi.org/10.1038/s41598-017-04102-z PubMedPubMedCentralGoogle Scholar
  24. 24.
    Feigin A, Leenders KL, Moeller JR, Missimer J, Kuenig G, Spetsieris P, Antonini A, Eidelberg D (2001) Metabolic network abnormalities in early Huntington's disease: an F-18 FDG PET study. J Nucl Med 42(1):1591–1595PubMedGoogle Scholar
  25. 25.
    Tang CC, Feigin A, Ma YL, Habeck C, Paulsen JS, Leenders KL, Teune LK, van Oostrom JCH, Guttman M, Dhawan V, Eidelberg D (2013) Metabolic network as a progression biomarker of premanifest Huntington's disease. J Clin Investig 123(9):4076–4088.  https://doi.org/10.1172/jci69411 PubMedGoogle Scholar
  26. 26.
    Guo Q, Jin L, Wu Y, Lv C (2007) Evaluation of Somato Symptom Self-Rating Scale. Nerv Dis Ment Health 7(2):91–94Google Scholar
  27. 27.
    Zung WW (1965) A self-rating depression scale. Arch Gen Psychiatry 12(1):63–70PubMedGoogle Scholar
  28. 28.
    Zung WW (1971) A rating instrument for anxiety disorders. Psychosomatics 12(6):371–379PubMedGoogle Scholar
  29. 29.
    Derrogatis L, Lipman R, Covi I (1973) The SCL-90: an outpatient psychiatric rating scale. Psychopharmacol Bull 9:13–28Google Scholar
  30. 30.
    Su J, Huang Q, Ren S, Xie F, Zhai Y, Guan Y, Liu J, Hua F (2019) Altered brain glucose metabolism assessed by 18F-FDG PET imaging is associated with the cognitive impairment of CADASIL. Neuroscience 417:35–44.  https://doi.org/10.1016/j.neuroscience.2019.07.048 PubMedGoogle Scholar
  31. 31.
    Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26(3):839–851.  https://doi.org/10.1016/j.neuroimage.2005.02.018 PubMedGoogle Scholar
  32. 32.
    Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15(1):273–289.  https://doi.org/10.1006/nimg.2001.0978 PubMedGoogle Scholar
  33. 33.
    Duan S, Mu X, Huang Q, Ma Y, Shan B (2018) Occult spastic diplegic cerebral palsy recognition using efficient machine learning for big data and structural connectivity abnormalities analysis. J Med Imaging Health Inform 8(2):317–324.  https://doi.org/10.1166/jmihi.2018.2282 Google Scholar
  34. 34.
    Zhang T, Huang Q, Jiao C, Liu H, Nie B, Liang S, Li P, Sun X, Feng T, Xu L, Shan B (2018) Modular architecture of metabolic brain network and its effects on the spread of perturbation impact. Neuroimage 186:146–154.  https://doi.org/10.1016/j.neuroimage.2018.11.003 PubMedGoogle Scholar
  35. 35.
    Hua J, Wenyuan W, Mingyuan Z (1986) Analysis of SCL-90 in Chinese norm (in Chinese version). Chin J Nerv Ment Dis 12(5):260–263Google Scholar
  36. 36.
    Chunfang W, Zehuan C, Qing X (1986) Self-rating depression scale of 1340 Chinese norm (in Chinese version). Chin J Nerv Ment Dis 5:267–268Google Scholar
  37. 37.
    Zhengyu W, Yufen C (1984) Self-rating anxiety scale (in Chinese version). Shanghai Arch Psychiatry 2:68–70Google Scholar
  38. 38.
    Koolschijn P, van Haren NEM, Lensvelt-Mulders G, Pol HEH, Kahn RS (2009) Brain volume abnormalities in major depressive disorder: a meta-analysis of magnetic resonance imaging studies. Hum Brain Mapp 30(11):3719–3735.  https://doi.org/10.1002/hbm.20801 PubMedGoogle Scholar
  39. 39.
    Fitzgerald PB, Laird AR, Maller J, Daskalakis ZJ (2008) A meta-analytic study of changes in brain activation in depression. Hum Brain Mapp 29(6):683–695.  https://doi.org/10.1002/hbm.20426 PubMedPubMedCentralGoogle Scholar
  40. 40.
    Hamilton JP, Furman DJ, Chang C, Thomason ME, Dennis E, Gotlib IH (2011) Default-mode and task-positive network activity in major depressive disorder: implications for adaptive and maladaptive rumination. Biol Psychiatry 70(4):327–333PubMedPubMedCentralGoogle Scholar
  41. 41.
    Saxena S, Brody AL, Schwartz JM, Baxter LR (1998) Neuroimaging and frontal-subcortical circuitry in obsessive-compulsive disorder. Br J Psychiatry Suppl 173(35):26Google Scholar
  42. 42.
    Saxena S, Rauch SL (2000) Functional neuroimaging and the neuroanatomy of obsessive–compulsive disorder. Psychiatr Clin N Am 23(3):563–586.  https://doi.org/10.1016/S0193-953X(05)70181-7 Google Scholar
  43. 43.
    Whiteside SP, Port JD, Abramowitz JS (2004) A meta-analysis of functional neuroimaging in obsessive–compulsive disorder. Psychiatry Res Neuroimaging 132(1):69–79.  https://doi.org/10.1016/j.pscychresns.2004.07.001 Google Scholar
  44. 44.
    Mataix-Cols D, Dorosario-Campos MC, Leckman JF (2005) A multidimensional model of obsessive–compulsive disorder. Am J Psychiatry 162(2):228–238PubMedGoogle Scholar
  45. 45.
    Menzies L, Chamberlain SR, Laird AR, Thelen SM, Sahakian BJ, Bullmore ET (2008) Integrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: the orbitofronto-striatal model revisited. Neurosci Biobehav Rev 32(3):525–549PubMedGoogle Scholar
  46. 46.
    Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24(1):167–202.  https://doi.org/10.1146/annurev.neuro.24.1.167 PubMedGoogle Scholar
  47. 47.
    Davidson RJ (2002) Anxiety and affective style: role of prefrontal cortex and amygdala. Biol Psychiatry 51(1):68–80.  https://doi.org/10.1016/S0006-3223(01)01328-2 PubMedGoogle Scholar
  48. 48.
    Sliz D, Hayley S (2012) Major depressive disorder and alterations in insular cortical activity: a review of current functional magnetic imaging research. Front Hum Neurosci.  https://doi.org/10.3389/fnhum.2012.00323 PubMedPubMedCentralGoogle Scholar
  49. 49.
    Joormann J, Gotlib IH (2010) Emotion regulation in depression: relation to cognitive inhibition. Cogn Emot 24(2):281–298PubMedPubMedCentralGoogle Scholar
  50. 50.
    Waller E, Scheidt CE (2006) Somatoform disorders as disorders of affect regulation: a development perspective. Int Rev Psychiatry 18(1):13–24.  https://doi.org/10.1080/09540260500466774 PubMedGoogle Scholar
  51. 51.
    McCarthy G, Puce A, Gore JC, Allison T (1997) Face-specific processing in the human fusiform gyrus. J Cogn Neurosci 9(5):605–610PubMedGoogle Scholar
  52. 52.
    Surguladze S, Brammer MJ, Keedwell P, Giampietro V, Young AW, Travis MJ, Williams SCR, Phillips ML (2005) A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biol Psychiatry 57(3):201–209.  https://doi.org/10.1016/j.biopsych.2004.10.028 PubMedGoogle Scholar
  53. 53.
    Osuch EA, Ketter TA, Kimbrell TA, George MS, Benson BE, Herscovitch MWW, Post RM (2000) Regional cerebral metabolism associated with anxiety symptoms in affective disorder patients. Biol Psychiatry 48(10):1020–1023.  https://doi.org/10.1016/S0006-3223(00)00920-3 PubMedGoogle Scholar
  54. 54.
    Seghier ML (2013) The angular gyrus: multiple functions and multiple subdivisions. Neuroscientist 19(1):43–61.  https://doi.org/10.1177/1073858412440596 PubMedPubMedCentralGoogle Scholar
  55. 55.
    Morecraft R, Geula C, Mesulam MM (1992) Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey. J Comp Neurol 323(3):341–358PubMedGoogle Scholar
  56. 56.
    Bremner JD, Vythilingam M, Vermetten E, Nazeer A, Adil J, Khan S, Staib LH, Charney DS (2002) Reduced volume of orbitofrontal cortex in major depression. Biol Psychiatry 51(4):273–279PubMedGoogle Scholar
  57. 57.
    Nakamura M, Nestor PG, Levitt JJ, Cohen AS, Kawashima T, Shenton ME, McCarley RW (2007) Orbitofrontal volume deficit in schizophrenia and thought disorder. Brain 131(1):180–195PubMedPubMedCentralGoogle Scholar
  58. 58.
    Koelsch S, Fritz T, Cramon DY, Müller K, Friederici AD (2006) Investigating emotion with music: an fMRI study. Human Brain Mapp 27(3):239–250Google Scholar
  59. 59.
    de Greck M, Scheidt L, Bolter AF, Frommer J, Ulrich C, Stockum E, Enzi B, Tempelmann C, Hoffmann T, Han SH, Northoff G (2012) Altered brain activity during emotional empathy in somatoform disorder. Hum Brain Mapp 33(11):2666–2685.  https://doi.org/10.1002/hbm.21392 PubMedGoogle Scholar
  60. 60.
    Bourke JH, Langford RM, White PD (2015) The common link between functional somatic syndromes may be central sensitisation. J Psychosom Res 78(3):228–236.  https://doi.org/10.1016/j.jpsychores.2015.01.003 PubMedGoogle Scholar
  61. 61.
    Kucyi A, Moayedi M, Weissman-Fogel I, Goldberg MB, Freeman BV, Tenenbaum HC, Davis KD (2014) Enhanced medial prefrontal-default mode network functional connectivity in chronic pain and its association with pain rumination. J Neurosci 34(11):3969–3975.  https://doi.org/10.1523/jneurosci.5055-13.2014 PubMedPubMedCentralGoogle Scholar
  62. 62.
    Brooks J, Tracey I (2007) The insula: a multidimensional integration site for pain. Pain 128(1):1–2PubMedGoogle Scholar
  63. 63.
    Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214(5–6):655–667PubMedPubMedCentralGoogle Scholar
  64. 64.
    Stankewitz A, Sorg C, von Kalckreuth A, Schulz E, Valet M, Neufang S, Zimmer C, Henningsen P, Guendel H, Wohlschlaeger AM, Toelle TR (2018) Fronto-insular connectivity during pain distraction is impaired in patients with somatoform pain. J Neuroimaging 28(6):621–628.  https://doi.org/10.1111/jon.12547 PubMedGoogle Scholar
  65. 65.
    Wiech K, Ploner M, Tracey I (2008) Neurocognitive aspects of pain perception. Trends Cogn Sci 12(8):306–313PubMedGoogle Scholar
  66. 66.
    Besteher B, Gaser C, Langbein K, Dietzek M, Sauer H, Nenadic I (2017) Effects of subclinical depression, anxiety and somatization on brain structure in healthy subjects. J Affect Disord 215:111–117.  https://doi.org/10.1016/j.jad.2017.03.039 PubMedGoogle Scholar
  67. 67.
    Bresch A, Rullmann M, Luthardt J, Arelin K, Becker GA, Patt M, Lobsien D, Baldofski S, Drabe M, Zeisig V, Regenthal R, Blueher M, Hilbert A, Sabri O, Hesse S (2016) In-vivo serotonin transporter availability and somatization in healthy subjects. Personality Individ Differ 94:354–359.  https://doi.org/10.1016/j.paid.2016.01.042 Google Scholar
  68. 68.
    Haruno M, Kawato M (2006) Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J Neurophysiol 95(2):948–959PubMedGoogle Scholar
  69. 69.
    Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW (2003) Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6:115.  https://doi.org/10.1038/nn1003 PubMedGoogle Scholar
  70. 70.
    Stoeter P, Bauermann T, Nickel R, Corluka L, Gawehn J, Vucurevic G, Vossel G, Egle U (2007) Cerebral activation in patients with somatoform pain disorder exposed to pain and stress: an fMRI study. Neuroimage 36(2):418–430PubMedGoogle Scholar
  71. 71.
    Blair R, Morris JS, Frith CD, Perrett DI, Dolan RJ (1999) Dissociable neural responses to facial expressions of sadness and anger. Brain 122(5):883–893PubMedGoogle Scholar
  72. 72.
    Hakala M, Karlsson H, Kurki T, Aalto S, Koponen S, Vahlberg T, Niemi PM (2004) Volumes of the caudate nuclei in women with somatization disorder and healthy women. Psychiatry Res Neuroimaging 131(1):71–78.  https://doi.org/10.1016/j.pscychresns.2004.03.001 Google Scholar
  73. 73.
    Rasmussen NH, Avant RF (1989) Somatization disorder in family practice. Am Fam Physician 40(2):206–214PubMedGoogle Scholar
  74. 74.
    Vuilleumier P, Chicherio C, Assal F, Schwartz S, Slosman D, Landis T (2001) Functional neuroanatomical correlates of hysterical sensorimotor loss. Brain 124(6):1077–1090.  https://doi.org/10.1093/brain/124.6.1077 PubMedGoogle Scholar
  75. 75.
    Egloff N, Sabbioni MEE, Salathe C, Wiest R, Juengling FD (2009) Nondermatomal somatosensory deficits in patients with chronic pain disorder: clinical findings and hypometabolic pattern in FDG-PET. Pain 145(1–2):252–258.  https://doi.org/10.1016/j.pain.2009.04.016 PubMedGoogle Scholar
  76. 76.
    Yoo HK, Kim MJ, Kim SJ, Sung YH, Sim ME, Lee YS, Song SY, Kee BS, Lyoo IK (2005) Putaminal gray matter volume decrease in panic disorder: an optimized voxel-based morphometry study. Eur J Neurosci 22(8):2089–2094.  https://doi.org/10.1111/j.1460-9568.2005.04394.x PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.PET Center, Huashan HospitalFudan UniversityShanghaiChina
  2. 2.Department of Psychiatry, Tianjin Anding HospitalTianjin Mental Health CenterTianjinChina
  3. 3.Department of Nuclear Medicine, Longhua HospitalShanghai University of Traditional Chinese MedicineShanghaiChina

Personalised recommendations