Overlapping and distinct neural metabolic patterns related to impulsivity and hypomania in Parkinson’s disease

  • Frank Schwartz
  • Masoud Tahmasian
  • Franziska Maier
  • Luisa Rochhausen
  • Kim L. Schnorrenberg
  • Fateme Samea
  • Joseph Seemiller
  • Mojtaba Zarei
  • Christian Sorg
  • Alexander Drzezga
  • Lars Timmermann
  • Thomas D. Meyer
  • Thilo van Eimeren
  • Carsten Eggers


Impulsivity and hypomania are common non-motor features in Parkinson’s disease (PD). The aim of this study was to find the overlapping and distinct neural correlates of these symptoms in PD. Symptoms of impulsivity and hypomania were assessed in 24 PD patients using the Barratt Impulsiveness Scale (BIS-11) and Self-Report Manic Inventory (SRMI), respectively. In addition, fluorodeoxyglucose positron emission tomography (FDG-PET) imaging for each individual was performed. We conducted two separate multiple regression analyses for BIS-11 and SRMI scores with FDG-PET data to identify the brain regions that are associated with both impulsivity and hypomania scores, as well as those exclusive to each symptom. Then, seed-based functional connectivity analyses on healthy subjects identified the areas connected to each of the exclusive regions and the overlapping region, used as seeds. We observed a positive association between BIS-11 and SRMI scores and neural metabolism only in the prefrontal areas. Conjunction analysis revealed an overlapping region in the middle frontal gyrus. Regions exclusive to impulsivity were found in the medial part of the right superior frontal gyrus and regions exclusive to hypomania were in the right superior frontal gyrus, right precentral gyrus and right paracentral lobule. Connectivity patterns of seeds exclusively related to impulsivity were different from those for hypomania in healthy brains. These results provide evidence of both overlapping and distinct regions linked with impulsivity and hypomania scores in PD. The exclusive regions for each characteristic are connected to specific intrinsic functional networks.


Impulsivity Hypomania Parkinson’s disease FDG-PET Functional connectivity 



We would like to thank all patients for their participation in the study. Moreover, we wish to thank the staff of the Departments of Neurology, University Hospital of Cologne, as well as Max Planck institute for Metabolism Research for their help in data collection.


This study was supported by the German Research Foundation (KFO 219 (TP10) and EI 892 3-1).

Compliance with ethical standards

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Ethical approval

Registration and ethical approval conforming to Human Research Committee guidelines was obtained by the medical ethics board of the University Hospital of Cologne (EK 10-278).

Informed consent

Written informed consent was obtained from all participants included in this study.


  1. Abosch, A., Gupte, A., Eberly, L. E., Tuite, P. J., Nance, M., & Grant, J. E. (2011). Impulsive behavior and associated clinical variables in Parkinson’s disease. Psychosomatics, 52(1), 41–47. Scholar
  2. Angst, J., Adolfsson, R., Benazzi, F., Gamma, A., Hantouche, E., Meyer, T. D., et al. (2005). The HCL-32: towards a self-assessment tool for hypomanic symptoms in outpatients. Journal of Affective Disorders, 88(2), 217–233. Scholar
  3. Bechara, A. (2005). Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nature Neuroscience, 8(11), 1458–1463. Scholar
  4. Bechara, A., & Van Der Linden, M. (2005). Decision-making and impulse control after frontal lobe injuries. Current Opinion in Neurobiology, 18(6), 734–739.CrossRefGoogle Scholar
  5. Beck, A. T., Steer, R. A., Ball, R., & Ranieri, W. (1996). Comparison of beck depression inventories -IA and -II in psychiatric outpatients. J Pers Assess, 67(3), 588–597. Scholar
  6. Berlin, H. A., Rolls, E. T., & Iversen, S. D. (2005). Borderline personality disorder, impulsivity, and the orbitofrontal cortex. American Journal of Psychiatry, 162(12), 2360–2373. Scholar
  7. Blumberg, H. P., Stern, E., Martinez, D., Ricketts, S., de Asis, J., White, T., et al. (2000). Increased anterior cingulate and caudate activity in bipolar mania. Biological Psychiatry, 48(11), 1045–1052.PubMedCrossRefGoogle Scholar
  8. Boes, A. D., Bechara, A., Tranel, D., Anderson, S. W., Richman, L., & Nopoulos, P. (2009). Right ventromedial prefrontal cortex: a neuroanatomical correlate of impulse control in boys. Social Cognitive and Affective Neuroscience, 4(1), 1–9. Scholar
  9. Brown, M. R., Benoit, J. R., Juhas, M., Dametto, E., Tse, T. T., MacKay, M., et al. (2015). fMRI investigation of response inhibition, emotion, impulsivity, and clinical high-risk behavior in adolescents. Frontiers in Systems Neuroscience, 9, 124. Scholar
  10. Buckner, R. L., Andrews-Hanna, J. R., & Schacter, D. L. (2008). The brain’s default network: anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124, 1–38. Scholar
  11. Caligiuri, M. P., Brown, G. G., Meloy, M. J., Eyler, L. T., Kindermann, S. S., Eberson, S., et al. (2004). A functional magnetic resonance imaging study of cortical asymmetry in bipolar disorder. Bipolar Disorders, 6(3), 183–196. Scholar
  12. Ceravolo, R., Frosini, D., Rossi, C., & Bonuccelli, U. (2009). Impulse control disorders in Parkinson’s disease: definition, epidemiology, risk factors, neurobiology and management. Parkinsonism & Related Disorders, 15 Suppl 4, 111–115. Scholar
  13. Chaudhuri, K. R., Healy, D. G., & Schapira, A. H. & National Institute for Clinical, E. (2006). Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurology, 5(3), 235–245,
  14. Choe, I. H., Yeo, S., Chung, K. C., Kim, S. H., & Lim, S. (2013). Decreased and increased cerebral regional homogeneity in early Parkinson’s disease. Brain Research, 1527, 230–237. Scholar
  15. Chopra, A., Tye, S. J., Lee, K. H., Sampson, S., Matsumoto, J., Adams, A., et al. (2012). Underlying neurobiology and clinical correlates of mania status after subthalamic nucleus deep brain stimulation in Parkinson’s disease: a review of the literature. The Journal of Neuropsychiatry and Clinical Neurosciences, 24(1), 102–110. Scholar
  16. Cilia, R., Siri, C., Marotta, G., Isaias, I. U., De Gaspari, D., Canesi, M., et al. (2008). Functional abnormalities underlying pathological gambling in Parkinson disease. Archives of Neurology, 65(12), 1604–1611. Scholar
  17. Cilia, R., & van Eimeren, T. (2011). Impulse control disorders in Parkinson’s disease: seeking a roadmap toward a better understanding. Brain Structure & Function, 216(4), 289–299. Scholar
  18. Coenen, V. A., Honey, C. R., Hurwitz, T., Rahman, A. A., McMaster, J., Burgel, U., et al. (2009). Medial forebrain bundle stimulation as a pathophysiological mechanism for hypomania in subthalamic nucleus deep brain stimulation for Parkinson’s disease. Neurosurgery, 64(6), 1106–1114. discussion 1114 – 1105.PubMedCrossRefGoogle Scholar
  19. Crunelle, C. L., Kaag, A. M., van Wingen, G., van den Munkhof, H. E., Homberg, J. R., Reneman, L., et al. (2014). Reduced frontal brain volume in non-treatment-seeking cocaine-dependent individuals: exploring the role of impulsivity, depression, and smoking. Frontiers in Human Neuroscience, 8, 7. Scholar
  20. Dagher, A., & Robbins, T. W. (2009). Personality, addiction, dopamine: insights from Parkinson’s disease. Neuron, 61(4), 502–510. Scholar
  21. Dalley, J. W., Everitt, B. J., & Robbins, T. W. (2011). Impulsivity, compulsivity, and top-down cognitive control. Neuron, 69(4), 680–694. Scholar
  22. Diener, H. C., & Putzki, N. (2008). Leitlinien für Diagnostik und Therapie in der Neurologie 4. Stuttgart: Georg Thieme Verlag.CrossRefGoogle Scholar
  23. Ding, W. N., Sun, J. H., Sun, Y. W., Chen, X., Zhou, Y., Zhuang, Z. G., et al. (2014). Trait impulsivity and impaired prefrontal impulse inhibition function in adolescents with internet gaming addiction revealed by a Go/No-Go fMRI study. Behavioral and Brain Functions, 10, 20. Scholar
  24. Eggers, C., Hilker, R., Burghaus, L., Schumacher, B., & Heiss, W. D. (2009). High resolution positron emission tomography demonstrates basal ganglia dysfunction in early Parkinson’s disease. Journal of the Neurological Sciences, 276(1–2), 27–30. Scholar
  25. Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., et al. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage, 25(4), 1325–1335. Scholar
  26. Evenden, J. L. (1999). Varieties of impulsivity. Psychopharmacology (Berlin), 146(4), 348–361.CrossRefGoogle Scholar
  27. Fahn, S., Elton, R., Committee, E. R. UD (1987). Unified Parkinson’s disease rating scale. In S. Fahn, C. Marsden, D. Calne, M. Goldstein (Ed.), Recent developments in Parkinson’s disease (pp. 153–163). Flora Park: MacMillan Healthcare Information.Google Scholar
  28. Fleck, D. E., Kotwal, R., Eliassen, J. C., Lamy, M., Delbello, M. P., Adler, C. M., et al. (2011). Preliminary evidence for increased frontosubcortical activation on a motor impulsivity task in mixed episode bipolar disorder. Journal of Affective Disorders, 133(1–2), 333–339. Scholar
  29. Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S., & Turner, R. (1996). Movement-related effects in fMRI time-series. Magnetic Resonance in Medicine, 35(3), 346–355.PubMedCrossRefGoogle Scholar
  30. Hoehn, M. M., & Yahr, M. D. (1967). Parkinsonism: onset, progression and mortality. Neurology, 17(5), 427–442.PubMedCrossRefGoogle Scholar
  31. Hughes, A. J., Ben-Shlomo, Y., Daniel, S. E., & Lees, A. J. (1992). What features improve the accuracy of clinical diagnosis in Parkinson’s disease: a clinicopathologic study. Neurology, 42(6), 1142–1146.PubMedCrossRefGoogle Scholar
  32. Ikemoto, S. (2010). Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory. Neuroscience and Biobehavioral Reviews, 35(2), 129–150. Scholar
  33. Inuggi, A., Sanz-Arigita, E., Gonzalez-Salinas, C., Valero-Garcia, A. V., Garcia-Santos, J. M., & Fuentes, L. J. (2014). Brain functional connectivity changes in children that differ in impulsivity temperamental trait. Frontiers in Behavioral Neuroscience, 8, 156. Scholar
  34. Jankovic, J. (2008). Parkinson’s disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry, 79(4), 368–376. Scholar
  35. Japee, S., Holiday, K., Satyshur, M. D., Mukai, I., & Ungerleider, L. G. (2015). A role of right middle frontal gyrus in reorienting of attention: a case study. Frontiers in Systems Neuroscience, 9, 23. Scholar
  36. Jentsch, J. D., & Taylor, J. R. (1999). Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology (Berlin), 146(4), 373–390.CrossRefGoogle Scholar
  37. Johnson, S. L., Carver, C. S., Mule, S., & Joormann, J. (2013). Impulsivity and risk for mania: towards greater specificity. Psychology and Psychotherapy, 86(4), 401–412. Scholar
  38. Kessler, J., Markowitsch, H. J., & Denzler, P. (2000). Mini-mental-status-test(MMST). Göttingen: Beltz Test GMBH.Google Scholar
  39. Kim, J. S., Kim, H. J., Lee, J. Y., Kim, J. M., Yun, J. Y., & Jeon, B. S. (2012). Hypomania induced by subthalamic nucleus stimulation in a Parkinson’s disease patient: does it suggest a dysfunction of the limbic circuit? Journal of Movement Disorders, 5(1), 14–17. Scholar
  40. Kim, S., & Lee, D. (2011). Prefrontal cortex and impulsive decision making. Biological Psychiatry, 69(12), 1140–1146. Scholar
  41. Kluetsch, R. C., Schmahl, C., Niedtfeld, I., Densmore, M., Calhoun, V. D., Daniels, J., et al. (2012). Alterations in default mode network connectivity during pain processing in borderline personality disorder. Archives of General Psychiatry, 69(10), 993–1002. Scholar
  42. Klupp, E., Grimmer, T., Tahmasian, M., Sorg, C., Yakushev, I., Yousefi, B. H., et al. (2015). Prefrontal hypometabolism in Alzheimer disease is related to longitudinal Amyloid accumulation in remote brain regions. Journal of Nuclear Medicine, 56(3), 399–404. Scholar
  43. Kriegeskorte, N., Simmons, W. K., Bellgowan, P. S., & Baker, C. I. (2009). Circular analysis in systems neuroscience: the dangers of double dipping. Nature Neuroscience, 12(5), 535–540. Scholar
  44. Kruger, S., Braunig, P., Shugar, G. (1997). Manie-Selbstbeurteilungsskala: MSS ; deutsche Bearbeitung des Self-Report manic inventory (SRMI). Göttingen: Beltz-Test.Google Scholar
  45. Kühner, C., Bürger, C., Keller, F., & Hautzinger, M. (2007). Reliability and validity of the Revised Beck Depression Inventory (BDI-II). Results from German samples. Nervenarzt, 78(6), 651–656. Scholar
  46. Kuo, M. F., Paulus, W., & Nitsche, M. A. (2014). Therapeutic effects of non-invasive brain stimulation with direct currents (tDCS) in neuropsychiatric diseases. NeuroImage, 85 Pt 3, 948–960. Scholar
  47. Kupferschmidt, D. A., & Zakzanis, K. K. (2011). Toward a functional neuroanatomical signature of bipolar disorder: quantitative evidence from the neuroimaging literature. Psychiatry Research, 193(2), 71–79. Scholar
  48. Langan, C., & McDonald, C. (2009). Neurobiological trait abnormalities in bipolar disorder. Molecular Psychiatry, 14(9), 833–846. Scholar
  49. Lee, S. K., Chun, J. W., Lee, J. S., Park, H. J., Jung, Y. C., Seok, J. H., et al. (2014). Abnormal neural processing during emotional salience attribution of affective asymmetry in patients with schizophrenia. PLoS One, 9(3), e90792. Scholar
  50. Lucignani, G., & Nobili, F. (2010). FDG-PET for early assessment of Alzheimer’s disease: isn’t the evidence base large enough? European Journal of Nuclear Medicine and Molecular Imaging, 37(8), 1604–1609. Scholar
  51. Maier, F., Merkl, J., Ellereit, A. L., Lewis, C. J., Eggers, C., Pedrosa, D. J., et al. (2014). Hypomania and mania related to dopamine replacement therapy in Parkinson’s disease. Parkinsonism & Related Disorders, 20(4), 421–427. Scholar
  52. Maier, F., Williamson, K. L., Tahmasian, M., Rochhausen, L., Ellereit, A. L., Prigatano, G. P., et al. (2016). Behavioural and neuroimaging correlates of impaired self-awareness of hypo- and hyperkinesia in Parkinson’s disease. Cortex, 82, 35–47. Scholar
  53. Manoliu, A., Meng, C., Brandl, F., Doll, A., Tahmasian, M., Scherr, M., et al. (2013). Insular dysfunction within the salience network is associated with severity of symptoms and aberrant inter-network connectivity in major depressive disorder. Frontiers in Human Neuroscience, 7, 930. Scholar
  54. Mason, L., O’Sullivan, N., Blackburn, M., Bentall, R., & El-Deredy, W. (2012). I want it now! Neural correlates of hypersensitivity to immediate reward in hypomania. Biological Psychiatry, 71(6), 530–537. Scholar
  55. Matsuo, K., Nicoletti, M., Nemoto, K., Hatch, J. P., Peluso, M. A., Nery, F. G., et al. (2009). A voxel-based morphometry study of frontal gray matter correlates of impulsivity. Human Brain Mapping, 30(4), 1188–1195. Scholar
  56. Mitchell, M. R., & Potenza, M. N. (2014). Recent insights into the neurobiology of impulsivity. Current Addiction Reports, 1(4), 309–319. Scholar
  57. Newman, A. L., & Meyer, T. D. (2014). Impulsivity: present during euthymia in bipolar disorder? - a systematic review. International Journal of Bipolar Disorders, 2, 2, Scholar
  58. Ongur, D., Lundy, M., Greenhouse, I., Shinn, A. K., Menon, V., Cohen, B. M., et al. (2010). Default mode network abnormalities in bipolar disorder and schizophrenia. Psychiatry Research, 183(1), 59–68. Scholar
  59. Opara, J. A., Brola, W., Leonardi, M., & Blaszczyk, B. (2012). Quality of life in Parkinson’s disease. Journal of Medicine and Life, 5(4), 375–381.PubMedPubMedCentralGoogle Scholar
  60. Patton, J. H., Stanford, M. S., & Barratt, E. S. (1995). Factor structure of the Barratt impulsiveness scale. Journal of Clinical Psychology, 51(6), 768–774.<768::Aid-Jclp2270510607>3.0.Co;2-1.PubMedCrossRefGoogle Scholar
  61. Power, J. D., Schlaggar, B. L., & Petersen, S. E. (2015). Recent progress and outstanding issues in motion correction in resting state fMRI. Neuroimage, 105, 536–551. Scholar
  62. Probst, C. C., & van Eimeren, T. (2013). The functional anatomy of impulse control disorders. Current Neurology and Neuroscience Reports, 13(10), 386. Scholar
  63. Sebastian, A., Jung, P., Krause-Utz, A., Lieb, K., Schmahl, C., & Tuscher, O. (2014). Frontal dysfunctions of impulse control - a systematic review in borderline personality disorder and attention-deficit/hyperactivity disorder. Frontiers in Human Neuroscience, 8, 698. Scholar
  64. Sheline, Y. I., Price, J. L., Yan, Z., & Mintun, M. A. (2010). Resting-state functional MRI in depression unmasks increased connectivity between networks via the dorsal nexus. Proceedings of the National Academy of Sciences of the United States of America, 107(24), 11020–11025. Scholar
  65. Shugar, G., Schertzer, S., Toner, B. B., & Di Gasbarro, I. (1992). Development, use, and factor analysis of a self-report inventory for mania. Comprehensive Psychiatry, 33(5), 325–331.PubMedCrossRefGoogle Scholar
  66. Soloff, P., Nutche, J., Goradia, D., & Diwadkar, V. (2008). Structural brain abnormalities in borderline personality disorder: a voxel-based morphometry study. Psychiatry Research, 164(3), 223–236. Scholar
  67. Strakowski, S. M., Adler, C. M., Cerullo, M., Eliassen, J. C., Lamy, M., Fleck, D. E., et al. (2008). Magnetic resonance imaging brain activation in first-episode bipolar mania during a response inhibition task. Early Intervention in Psychiatry, 2(4), 225–233. Scholar
  68. Strakowski, S. M., Eliassen, J. C., Lamy, M., Cerullo, M. A., Allendorfer, J. B., Madore, M., et al. (2011). Functional magnetic resonance imaging brain activation in bipolar mania: evidence for disruption of the ventrolateral prefrontal-amygdala emotional pathway. Biological Psychiatry, 69(4), 381–388. Scholar
  69. Swann, A. C. (2009). Impulsivity in mania. Current Psychiatry Reports, 11(6), 481–487.PubMedCrossRefGoogle Scholar
  70. Tahmasian, M., Bettray, L. M., van Eimeren, T., Drzezga, A., Timmermann, L., Eickhoff, C. R., et al. (2015a). A systematic review on the applications of resting-state fMRI in Parkinson’s disease: does dopamine replacement therapy play a role? Cortex, 73, 80–105. Scholar
  71. Tahmasian, M., Pasquini, L., Scherr, M., Meng, C., Forster, S., Bratec, M., S., et al (2015b). The lower hippocampus global connectivity, the higher its local metabolism in Alzheimer disease. Neurology, 84(19), 1956–1963.
  72. Tahmasian, M., Rochhausen, L., Maier, F., Williamson, K. L., Drzezga, A., Timmermann, L., et al. (2015c). Impulsivity is associated with increased metabolism in the Fronto-insular network in Parkinson’s disease. Frontiers in Behavioral Neuroscience, 9, 317. Scholar
  73. Tahmasian, M., Shao, J., Meng, C., Grimmer, T., Diehl-Schmid, J., Yousefi, B. H., et al. (2016). Based on the network degeneration hypothesis: separating individual patients with different neurodegenerative syndromes in a preliminary hybrid PET/MR study. Journal of Nuclear Medicine, 57(3), 410–415. Scholar
  74. Tahmasian, M., Eickhoff, S.B., Giehl, K., Schwartz, F., Herz, D. M., Drzezga, A., van Eimeren, T., Laird, A. R., Fox, P. T., Zarei, M., Eggers, C., Eickhoff, C.R. (2017). Resting-state functional reorganization in Parkinson’s disease: an activation likelihood estimation meta-analysis. Cortex, 92, 119–138.
  75. Talati, A., & Hirsch, J. (2005). Functional specialization within the medial frontal gyrus for perceptual go/no-go decisions based on “what,” “when,” and “where” related information: an fMRI study. Journal of Cognitive Neuroscience, 17(7), 981–993. Scholar
  76. Townsend, J. D., Sugar, C. A., Walshaw, P. D., Vasquez, R. E., Foland-Ross, L. C., Moody, T. D., et al. (2013). Frontostriatal neuroimaging findings differ in patients with bipolar disorder who have or do not have ADHD comorbidity. Journal of Affective Disorders, 147(1–3), 389–396. Scholar
  77. Tracy, D. K., Shergill, S. S., David, A. S., Fonagy, P., Zaman, R., Downar, J., et al. (2015). Self-harm and suicidal acts: a suitable case for treatment of impulsivity-driven behaviour with repetitive transcranial magnetic stimulation (rTMS). BJPsych Open, 1(1), 87–91. Scholar
  78. Trost, S., Diekhof, E. K., Zvonik, K., Lewandowski, M., Usher, J., Keil, M., et al. (2014). Disturbed anterior prefrontal control of the mesolimbic reward system and increased impulsivity in bipolar disorder. Neuropsychopharmacology, 39(8), 1914–1923. Scholar
  79. Ulla, M., Thobois, S., Llorca, P. M., Derost, P., Lemaire, J. J., Chereau-Boudet, I., et al. (2011). Contact dependent reproducible hypomania induced by deep brain stimulation in Parkinson’s disease: clinical, anatomical and functional imaging study. Journal of Neurology, Neurosurgery, and Psychiatry, 82(6), 607–614. Scholar
  80. van Eimeren, T., Ballanger, B., Pellecchia, G., Miyasaki, J. M., Lang, A. E., & Strafella, A. P. (2009). Dopamine agonists diminish value sensitivity of the orbitofrontal cortex: a trigger for pathological gambling in Parkinson’s disease? Neuropsychopharmacology, 34(13), 2758–2766. Scholar
  81. van Eimeren, T., Pellecchia, G., Cilia, R., Ballanger, B., Steeves, T. D., Houle, S., et al. (2010). Drug-induced deactivation of inhibitory networks predicts pathological gambling in PD. Neurology, 75(19), 1711–1716. Scholar
  82. Voon, V., Gao, J., Brezing, C., Symmonds, M., Ekanayake, V., Fernandez, H., et al. (2011a). Dopamine agonists and risk: impulse control disorders in Parkinson’s disease. Brain, 134(Pt 5), 1438–1446. Scholar
  83. Voon, V., Sohr, M., Lang, A. E., Potenza, M. N., Siderowf, A. D., Whetteckey, J., et al. (2011b). Impulse control disorders in Parkinson disease: a multicenter case–control study. Annals of Neurology, 69(6), 986–996. Scholar
  84. Winstanley, C. A., Eagle, D. M., & Robbins, T. W. (2006). Behavioral models of impulsivity in relation to ADHD: translation between clinical and preclinical studies. Clinical Psychology Review, 26(4), 379–395. Scholar
  85. Winston, G. P., Stretton, J., Sidhu, M. K., Symms, M. R., Thompson, P. J., & Duncan, J. S. (2013). Structural correlates of impaired working memory in hippocampal sclerosis. Epilepsia, 54(7), 1143–1153. Scholar
  86. Worsley, K. J., Marrett, S., Neelin, P., Vandal, A. C., Friston, K. J., & Evans, A. C. (1996). A unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapping, 4(1), 58–73,<58::AID-HBM4>3.0.CO;2-OPubMedCrossRefGoogle Scholar
  87. Xu, X., Yuan, H., & Lei, X. (2016). Activation and connectivity within the default mode network contribute independently to future-oriented thought. Science Reports, 6, 21001. Scholar
  88. Yang, H., Li, L., Peng, H., Liu, T., Young, A. H., Angst, J., et al. (2016). Alterations in regional homogeneity of resting-state brain activity in patients with major depressive disorder screening positive on the 32-item hypomania checklist (HCL-32). Journal of Affective Disorders, 203, 69–76. Scholar
  89. Zhu, X., Cortes, C. R., Mathur, K., Tomasi, D., & Momenan, R. (2015). Model-free functional connectivity and impulsivity correlates of alcohol dependence: a resting-state study. Addiction Biology. Scholar
  90. Zou, K. H., Warfield, S. K., Bharatha, A., Tempany, C. M., Kaus, M. R., Haker, S. J., et al. (2004). Statistical validation of image segmentation quality based on a spatial overlap index. Academic Radiology, 11(2), 178–189.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Frank Schwartz
    • 1
  • Masoud Tahmasian
    • 2
  • Franziska Maier
    • 1
    • 3
  • Luisa Rochhausen
    • 1
  • Kim L. Schnorrenberg
    • 1
  • Fateme Samea
    • 4
  • Joseph Seemiller
    • 5
  • Mojtaba Zarei
    • 2
  • Christian Sorg
    • 6
    • 7
    • 8
  • Alexander Drzezga
    • 9
  • Lars Timmermann
    • 1
    • 3
  • Thomas D. Meyer
    • 10
  • Thilo van Eimeren
    • 1
    • 9
  • Carsten Eggers
    • 1
    • 3
  1. 1.Department of NeurologyUniversity Hospital CologneCologneGermany
  2. 2.Institute of Medical Science and TechnologyShahid Beheshti UniversityTehranIran
  3. 3.Department of NeurologyUniversity Hospital MarburgMarburgGermany
  4. 4.Institute for Cognitive and Brain SciencesShahid Beheshti UniversityTehranIran
  5. 5.Geisinger Commonwealth School of MedicineScrantonUSA
  6. 6.Departments of Neuroradiology, Klinikum rechts der IsarTechnische Universität MünchenMunichGermany
  7. 7.TUM-Neuroimaging Center (TUM-NIC)Technische Universität MünchenMunichGermany
  8. 8.Department of PsychiatryTechnische Universität MünchenMunichGermany
  9. 9.Department of Nuclear MedicineUniversity Hospital CologneCologneGermany
  10. 10.McGovern Medical School, Department of Psychiatry and Behavioral SciencesUniversity of Texas Health Science CenterHoustonUSA

Personalised recommendations