Advertisement

Brain Topography

, Volume 32, Issue 1, pp 87–96 | Cite as

Extraversion and Neuroticism Related to Topological Efficiency in White Matter Network: An Exploratory Study Using Diffusion Tensor Imaging Tractography

  • Yajing Pang
  • Heng Chen
  • Yuyan Chen
  • Qian CuiEmail author
  • Yifeng Wang
  • Zhiqiang Zhang
  • Guangming Lu
  • Huafu ChenEmail author
Original Paper
  • 217 Downloads

Abstract

White matter (WM) fibers underpin individual differences in extraversion and neuroticism. These personality traits are associated with integration of emotion, cognition, and behavior, which rely on a large-scale brain network. Thus, research at network level is needed to characterize neural underpinnings of extraversion and neuroticism. We performed diffusion tensor imaging on 68 healthy individuals and combined a WM network with graph theory analysis to investigate the connectivity of the whole-brain network and individual regions associated with extraversion and neuroticism. Extraversion was negatively associated with local efficiency in the medial prefrontal cortex (MPFC), and neuroticism was positively associated with local and global efficiencies mainly in the hippocampus and MPFC regions, respectively. These identified regions demonstrated connectivity with other cortical and subcortical regions. No reliable associations were found between the network local and global efficiencies and extraversion, as well as neuroticism. These findings indicated the association between specific personality dimensions and information transfer in the prefrontal–limbic regions, which provided further insight into the neural mechanism to characterize extraversion and neuroticism.

Keywords

Extraversion Neuroticism White matter network Graph theory analysis 

Notes

Acknowledgements

This work was supported by the Natural Science Foundation of China (61533006, 81771919, and 31600930), the Science Foundation of Ministry of Education of China (14XJC190003), and the Fundamental Research Funds for the Central Universities (ZYGX2013Z004, ZYGX2014J104, and ZYGX2016KYQD120).

Author Contributions

YP and HC conceived and designed the experiments. ZZ and GL prepared the samples. YP, HC, and YC analyzed the data. YP, QC, and YW participated in the interpretation of data. YP wrote the paper.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

10548_2018_665_MOESM1_ESM.docx (2.1 mb)
Supplementary material 1 (DOCX 2101 KB)

References

  1. Achard S, Bullmore E (2007) Efficiency and cost of economical brain functional networks. PLoS Comput Biol 3:e17CrossRefGoogle Scholar
  2. Alexander GE, MR DeLong, Strick PL (2003) Parallel organization of functionally segregated circuits linking basal ganglia and cortex annual. Rev Neurosci 9:357–381CrossRefGoogle Scholar
  3. Barrett LF, Satpute AB (2013) Large-scale brain networks in affective and social neuroscience: towards an integrative functional architecture of the brain. Curr Opin Neurobiol 23:361CrossRefGoogle Scholar
  4. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44:625–632CrossRefGoogle Scholar
  5. Bjørnebekk A, Westlye LT, Fjell AM, Grydeland H, Walhovd KB (2012) Social reward dependence and brain white matter microstructure. Cereb Cortex 22:2672–2679CrossRefGoogle Scholar
  6. Bjørnebekk A, Fjell AM, Walhovd KB, Grydeland H, Torgersen S, Westlye LT (2013) Neuronal correlates of the five factor model (FFM) of human personality: multimodal imaging in a large healthy sample. NeuroImage 65:194–208CrossRefGoogle Scholar
  7. Bressler SL, Menon V (2010) Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci 14:277CrossRefGoogle Scholar
  8. Burzynska AZ et al (2013) A scaffold for efficiency in the human brain. J Neurosci 33:17150–17159CrossRefGoogle Scholar
  9. Canli T (2004) Functional brain mapping of extraversion and neuroticism: learning from individual differences in emotion processing. J Personal 72:1105–1132CrossRefGoogle Scholar
  10. Chai XJ, Ofen N, Gabrieli JDE, Whitfield-Gabrieli S (2014) Selective development of anticorrelated networks in the intrinsic functional organization of the human brain. J Cogn Neurosci 26:501CrossRefGoogle Scholar
  11. Chen Z, Liu M, Gross DW, Christian B (2013) Graph theoretical analysis of developmental patterns of the white matter network. Front Hum Neurosci 7:716Google Scholar
  12. Clark LA, Watson D (2008) Temperament: an organizing paradigm for trait psychology. In: John OP, Robins RW, Pervin LA (eds) Handbook of personality: theory and research, 3rd edn. Guilford Press, New York, pp 265–286Google Scholar
  13. Costa PT, McCrae RR (1992) Revised NEO Personality Inventory (NEO-PI-R) and NEO Five-Factor Inventory (NEO-FFI) professional manual. Psychological Assessment Resources, OdessaGoogle Scholar
  14. Denkova E, Dolcos S, Dolcos F (2012) Reliving emotional personal memories: affective biases linked to personality and sex-related differences. Emotion 12:515–528CrossRefGoogle Scholar
  15. Johnson DL, Wiebe JS, Gold SM, Andreasen NC, Hichwa RD, Watkins GL, Boles Ponto LL (1999) Cerebral blood flow and personality: a positron emission tomography study. Am J Psychiatry 156:252Google Scholar
  16. Eysenck HJ (1967) The biological basis of personality, vol 689. Transaction Publishers, New BrunswickGoogle Scholar
  17. Eysenck HJ (1991) Manual of the Eysenck personality scales (EPS Adult). Hodder & Stoughton, LondonGoogle Scholar
  18. Eysenck HJ (1994) Personality: biological foundations. Academic Press, New YorkGoogle Scholar
  19. Fishman I, Ng R, Bellugi U (2011) Do extraverts process social stimuli differently from introverts? Cogn Neurosci 2:67–73CrossRefGoogle Scholar
  20. Fornito A, Yoon J, Zalesky A, Bullmore ET, Cs. C (2011) General and specific functional connectivity disturbances in first-episode schizophrenia during cognitive control performance. Biol Psychiatry 70:64–72CrossRefGoogle Scholar
  21. Fossati P, Hevenor SJ, Graham SJ, Grady C, Keightley ML, Craik F, Mayberg H (2003) In search of the emotional self: an fMRI study using positive and negative emotional words. Am J Psychiatry 160:1938–1945CrossRefGoogle Scholar
  22. Gao Q et al (2013) Extraversion and neuroticism relate to topological properties of resting-state brain networks. Front Hum Neurosci 7:257.  https://doi.org/10.3389/fnhum.2013.00257 Google Scholar
  23. Gong Y (1984) Eysenck personality questionnaire revised in China. Inf Psychol Sci 4:11–18Google Scholar
  24. Greenberg DL, Rice HJ, Cooper JJ, Cabeza R, Rubin DC, Labar KS (2005) Co-activation of the amygdala, hippocampus and inferior frontal gyrus during autobiographical memory retrieval. Neuropsychologia 43:659–674CrossRefGoogle Scholar
  25. Haas BW, Canli T (2008) Emotional memory function, personality structure and psychopathology: a neural system approach to the identification of vulnerability markers. Brain Res Rev 58:71–84CrossRefGoogle Scholar
  26. Haas BW, Constable RT, Canli T (2008) Stop the sadness: neuroticism is associated with sustained medial prefrontal cortex response to emotional facial expressions. Neuroimage 42:385–392CrossRefGoogle Scholar
  27. Heatherton TF (2011) Neuroscience of self and self-regulation. Annu Rev Psychol 62:363CrossRefGoogle Scholar
  28. Hooker CI, Verosky SC, Miyakawa A, Knight RT, D’Esposito M (2008) The influence of personality on neural mechanisms of observational fear and reward learning. Neuropsychologia 46:2709–2724CrossRefGoogle Scholar
  29. Johansen-Berg H (2010) Behavioural relevance of variation in white matter microstructure. Curr Opin Neurol 23:351–358Google Scholar
  30. Jones DK, Cercignani M (2010) Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed 23:803CrossRefGoogle Scholar
  31. Jorm AF (1987) Sex differences in neuroticism: a quantitative synthesis of published research. Aust NZ J Psychiatry 21:501–506CrossRefGoogle Scholar
  32. Katsumi Y, Denkova E, Dolcos S (2017) Personality and memory. In: Zeigler-Hill V, Shackelford TK (eds) Encyclopedia of personality and individual differences. Springer International Publishing, New York, NY, pp 1–9Google Scholar
  33. Kennis M, Rademaker AR, Geuze E (2013) Neural correlates of personality: an integrative review. Neurosci Biobehav Rev 37:73–95CrossRefGoogle Scholar
  34. Kochunov P et al (2013) Acute nicotine administration effects on fractional anisotropy of cerebral white matter and associated attention performance. Front Pharmacol 4:117CrossRefGoogle Scholar
  35. Koenis MM et al (2015) Development of the brain’s structural network efficiency in early adolescence: a longitudinal DTI twin study. Hum Brain Mapp 36:4938–4953CrossRefGoogle Scholar
  36. Kumari V, Ffytche DH, Williams SC, Gray JA (2004) Personality predicts brain responses to cognitive demands. J Neurosci 24:10636–10641CrossRefGoogle Scholar
  37. Kuyken W, Dalgleish T (2011) Overgeneral autobiographical memory in adolescents at risk for depression. Memory 19:241–250CrossRefGoogle Scholar
  38. Larsen RJ, Ketelaar T (1991) Personality and susceptibility to positive and negative emotional states. Journal of personality social psychology 61:132.  https://doi.org/10.1037/0022-3514.61.1.132 CrossRefGoogle Scholar
  39. Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87:198701CrossRefGoogle Scholar
  40. Lei D et al (2015) Connectome-scale assessments of functional connectivity in children with primary monosymptomatic nocturnal enuresis. BioMed Res Int.  https://doi.org/10.1155/2015/463708 Google Scholar
  41. Lewis JD et al (2013) Network inefficiencies in autism spectrum disorder at 24 months. Transl Psychiatry 4:e388CrossRefGoogle Scholar
  42. Liao W et al (2011) Default mode network abnormalities in mesial temporal lobe epilepsy: a study combining fMRI and DTI. Hum Brain Mapp 32:883–895CrossRefGoogle Scholar
  43. Liao W et al (2016) Functional connectome before and following temporal lobectomy in mesial temporal lobe epilepsy. Sci Rep 6:23153CrossRefGoogle Scholar
  44. Long Z et al (2013) Altered brain structural connectivity in post-traumatic stress disorder: a diffusion tensor imaging tractography study. J Affect Disord 150:798–806CrossRefGoogle Scholar
  45. Lynall ME, Bassett DR, Mckenna PJ, Kitzbichler M, Muller U, Bullmore E (2010) Functional connectivity and brain networks in schizophrenia. J Neurosci 30:9477–9487CrossRefGoogle Scholar
  46. Mitchell RLC, Kumari V (2016) Hans Eysenck’s interface between the brain and personality: modern evidence on the cognitive neuroscience of personality. Pers Individ Dif 103:74–81CrossRefGoogle Scholar
  47. Mitchell JP, Banaji MR, Macrae CN (2005) The link between social cognition and self-referential thought in the medial prefrontal cortex. J Cogn Neurosci 17:1306CrossRefGoogle Scholar
  48. Mori S, Wakana S, LM N-P PC, vZ (2005) MRI atlas of human white matter. Elsevier, AmsterdamGoogle Scholar
  49. Mp VDH, Stam CJ, Kahn RS, Hulshoff Pol HE (2009) Efficiency of functional brain networks and intellectual performance. J Neurosci 29:7619–7624CrossRefGoogle Scholar
  50. Neurology AO (1993) Frontal-subcortical circuits and human behavior. J Psychosom Res 44:627–628Google Scholar
  51. Nyberg L et al (2016) Dopamine D2 receptor availability is linked to hippocampal-caudate functional connectivity and episodic memory. Proc Natl Acad Sci USA 113:7918CrossRefGoogle Scholar
  52. Ochsner KN, Ray R, Cooper J, Robertson E, Chopra S, Gabrieli J, Gross J (2004) For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage 23:483CrossRefGoogle Scholar
  53. Ochsner KN, Beer JS, Robertson ER, Cooper JC, Gabrieli JD, Kihsltrom JF, D’Esposito M (2005) The neural correlates of direct and reflected self-knowledge. Neuroimage 28:797CrossRefGoogle Scholar
  54. Olaf S (2013) Structure and function of complex brain networks. Dialogues Clin Neurosci 15:247Google Scholar
  55. Oouchi H, Yamada K, Sakai K, Kizu O, Kubota T, Ito H, Nishimura T (2007) Diffusion anisotropy measurement of brain white matter is affected by voxel size: underestimation occurs in areas with crossing fibers. AJNR 28:1102–1106CrossRefGoogle Scholar
  56. Ormel J et al (2013) The biological and psychological basis of neuroticism: current status and future directions. Neurosci Biobehav Rev 37:59–72CrossRefGoogle Scholar
  57. Pang Y et al (2015) Extraversion modulates functional connectivity hubs of resting-state brain networks. J Neuropsychol 11(3):347–361CrossRefGoogle Scholar
  58. Pang Y et al (2016) Extraversion and neuroticism related to the resting-state effective connectivity of amygdala. Sci Rep 6:35484CrossRefGoogle Scholar
  59. Paul RH et al (2008) Chronic cigarette smoking and the microstructural integrity of white matter in healthy adults: a diffusion tensor imaging study. Nicotine Tob Res 10:137CrossRefGoogle Scholar
  60. Perkins AM, Arnone D, Smallwood J, Mobbs D (2015) Thinking too much: self-generated thought as the engine of neuroticism. Trends Cogn Sci 19:492CrossRefGoogle Scholar
  61. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59:2142–2154CrossRefGoogle Scholar
  62. Robinson MD, Meier BP (2005) Rotten to the core: neuroticism and implicit evaluations of the self. Self Identity 4:361–372CrossRefGoogle Scholar
  63. Robinson MD, Ode S, Moeller SK, Goetz PW (2007) Neuroticism and affective priming: evidence for a neuroticism-linked negative schema. Person Individ Diff 42:1221–1231CrossRefGoogle Scholar
  64. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. NeuroImage 52:1059–1069CrossRefGoogle Scholar
  65. Ruizcaballero JA, Bermúdez J (1995) Neuroticism, mood, and retrieval of negative personal memories. J Gen Psychol 122:29CrossRefGoogle Scholar
  66. Sadeh N, Spielberg JM, Warren SL, Miller GA, Heller W (2014) Aberrant neural connectivity during emotional processing associated with posttraumatic stress. Clin Psychol Sci A 2:748CrossRefGoogle Scholar
  67. Servaas MN, Geerligs L, Renken RJ, Marsman J-BC, Ormel J, Riese H, Aleman A (2015) Connectomics and neuroticism: an altered functional network organization. Neuropsychopharmacology 40:296–304CrossRefGoogle Scholar
  68. Shackman AJ, Mcmenamin BW, Maxwell JS, Greischar LL, Davidson RJ (2009) Right dorsolateral prefrontal cortical activity and behavioral inhibition. Psychol Sci 20:1500CrossRefGoogle Scholar
  69. Shu N, Liu Y, Li J, Li Y, Yu C, Jiang T (2009) Altered anatomical network in early blindness revealed by diffusion tensor tractography. PLoS ONE.  https://doi.org/10.1371/journal.pone.0007228 Google Scholar
  70. Smith SM (2012) The future of FMRI connectivity. NeuroImage 62:1257–1266CrossRefGoogle Scholar
  71. Tzourio-Mazoyer N et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15:273–289.  https://doi.org/10.1006/nimg.2001.0978 CrossRefGoogle Scholar
  72. van den Heuvel MP, Kahn RS, Goñi J, Sporns O (2012) High-cost, high-capacity backbone for global brain communication. Proc Natl Acad Sci USA 109:11372–11377CrossRefGoogle Scholar
  73. Vianello M, Schnabel K, Sriram N, Nosek B (2013) Gender differences in implicit and explicit personality traits. Pers Individ Diff 55:994–999CrossRefGoogle Scholar
  74. Wang R, Benner T, Sorensen A, Wedeen V (2007) Diffusion toolkit: a software package for diffusion imaging data processing and tractography. In: Proceedings of the International Society for Magnetic Resonance in Medicine, vol. 3720Google Scholar
  75. Wei L et al (2011) The synchronization of spontaneous BOLD activity predicts extraversion and neuroticism. Brain Res 1419:68–75.  https://doi.org/10.1016/j.brainres.2011.08.060 CrossRefGoogle Scholar
  76. Weisberg YJ, Deyoung CG, Hirsh JB (2011) Gender differences in personality across the ten aspects of the big five. Front Psychol 2:178CrossRefGoogle Scholar
  77. Wen W et al (2011) Discrete neuroanatomical networks are associated with specific cognitive abilities in old age. J Neurosci 31:1204–1212CrossRefGoogle Scholar
  78. Wright CI, Williams D, Feczko E, Barrett LF, Dickerson BC, Schwartz CE, Wedig MM (2006) Neuroanatomical correlates of extraversion and neuroticism. Cereb Cortex 16:1809–1819CrossRefGoogle Scholar
  79. Xu J, Potenza MN (2012) White matter integrity and five-factor personality. Meas Healthy Adults NeuroImage 59:800–807Google Scholar
  80. Yamada H et al (2014) Efficacy of distortion correction on diffusion imaging: comparison of FSL Eddy and Eddy_Correct using 30 and 60 directions diffusion encoding. PLoS ONE 9:e112411CrossRefGoogle Scholar
  81. Zhang Z et al (2011) Altered functional–structural coupling of large-scale brain networks in idiopathic generalized epilepsy. Brain 134:2912–2928CrossRefGoogle Scholar
  82. Zhong S, He Y, Gong G (2015) Convergence and divergence across construction methods for human brain white matter networks: an assessment based on individual differences. Hum Brain Mapp 36:1995–2013CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for NeuroinformationUniversity of Electronic Science and Technology of ChinaChengduChina
  2. 2.School of Life Science and Technology, Center for Information in MedicineUniversity of Electronic Science and Technology of ChinaChengduChina
  3. 3.School of Public AdministrationUniversity of Electronic Science and Technology of ChinaChengduChina
  4. 4.Department of Medical Imaging, Jinling HospitalNanjing University School of MedicineNanjingChina

Personalised recommendations