Brain Structure and Function

, Volume 219, Issue 5, pp 1673–1684 | Cite as

Physiological and psychological individual differences influence resting brain function measured by ASL perfusion

  • M. Kano
  • S. J. Coen
  • A. D. Farmer
  • Q. Aziz
  • S. C. R. Williams
  • D. C. Alsop
  • S. Fukudo
  • R. L. O’GormanEmail author
Original Article


Effects of physiological and/or psychological inter-individual differences on the resting brain state have not been fully established. The present study investigated the effects of individual differences in basal autonomic tone and positive and negative personality dimensions on resting brain activity. Whole-brain resting cerebral perfusion images were acquired from 32 healthy subjects (16 males) using arterial spin labeling perfusion MRI. Neuroticism and extraversion were assessed with the Eysenck Personality Questionnaire-Revised. Resting autonomic activity was assessed using a validated measure of baseline cardiac vagal tone (CVT) in each individual. Potential associations between the perfusion data and individual CVT (27 subjects) and personality score (28 subjects) were tested at the level of voxel clusters by fitting a multiple regression model at each intracerebral voxel. Greater baseline perfusion in the dorsal anterior cingulate cortex (ACC) and cerebellum was associated with lower CVT. At a corrected significance threshold of p < 0.01, strong positive correlations were observed between extraversion and resting brain perfusion in the right caudate, brain stem, and cingulate gyrus. Significant negative correlations between neuroticism and regional cerebral perfusion were identified in the left amygdala, bilateral insula, ACC, and orbitofrontal cortex. These results suggest that individual autonomic tone and psychological variability influence resting brain activity in brain regions, previously shown to be associated with autonomic arousal (dorsal ACC) and personality traits (amygdala, caudate, etc.) during active task processing. The resting brain state may therefore need to be taken into account when interpreting the neurobiology of individual differences in structural and functional brain activity.


MRI Perfusion Autonomic nervous system Personality Cerebral blood flow 


  1. Aguirre GK, Detre JA, Zarahn E, Alsop DC (2002) Experimental design and the relative sensitivity of BOLD and perfusion fMRI. Neuroimage 15(3):488–500. doi: 10.1006/nimg.2001.0990 PubMedCrossRefGoogle Scholar
  2. Alsop DC, Detre JA (1998) Multisection cerebral blood flow MR imaging with continuous arterial spin labeling. Radiology 208(2):410–416PubMedCrossRefGoogle Scholar
  3. Canli T (2004a) Functional brain mapping of extraversion and neuroticism: learning from individual differences in emotion processing. J Pers 72(6):1105–1132PubMedCrossRefGoogle Scholar
  4. Canli T, Amin Z, Haas B, Omura K, Constable RT (2004b) A double dissociation between mood states and personality traits in the anterior cingulate. Behav Neurosci 118(5):897–904PubMedCrossRefGoogle Scholar
  5. Cardenas CG, Mar LP, Vysokanov AV, Arnold PB, Cardenas LM, Surmeier DJ, Scroggs RS (1999) Serotonergic modulation of hyperpolarization-activated current in acutely isolated rat dorsal root ganglion neurons. J Physiol 518(Pt 2):507–523PubMedCentralPubMedCrossRefGoogle Scholar
  6. Carney RM, Freedland KE, Veith RC (2005) Depression, the autonomic nervous system, and coronary heart disease. Psychosom Med 67(Suppl 1):S29–S33PubMedCrossRefGoogle Scholar
  7. Coen SJ, Kano M, Farmer AD, Kumari V, Giampietro V, Brammer M, Williams SC, Aziz Q (2011) Neuroticism influences brain activity during the experience of visceral pain. Gastroenterology 141(3):909–917PubMedCrossRefGoogle Scholar
  8. Critchley HD (2005) Neural mechanisms of autonomic, affective, and cognitive integration. J Comp Neurol 493(1):154–166PubMedCrossRefGoogle Scholar
  9. Critchley HD (2009) Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. Int J Psychophysiol 73(2):88–94PubMedCentralPubMedCrossRefGoogle Scholar
  10. Dai W, Garcia D, de Bazelaire C, Alsop DC (2008) Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn Reson Med 60(6):1488–1497PubMedCentralPubMedCrossRefGoogle Scholar
  11. Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW (2007) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9(1):46–56CrossRefGoogle Scholar
  12. Deckersbach T, Miller KK, Klibanski A, Fischman A, Dougherty DD, Blais MA, Herzog DB, Rauch SL (2006) Regional cerebral brain metabolism correlates of neuroticism and extraversion. Depress Anxiety 23(3):133–138PubMedCrossRefGoogle Scholar
  13. Deegan BM, Devine ER, Geraghty MC, Jones E, Ólaighin G, Serrador JM (2010) The relationship between cardiac output and dynamic cerebral autoregulation in humans. J Appl Physiol 109(5):1424–1431PubMedCentralPubMedCrossRefGoogle Scholar
  14. Depue RA, Collins PF (1999) Neurobiology of the structure of personality: dopamine, facilitation of incentive motivation, and extraversion. Behav Brain Sci 22(3):491–517 discussion 518–469PubMedGoogle Scholar
  15. Detre JA, Leigh JS, Williams DS, Koretsky AP (1992) Perfusion Imaging. Magnet Reson Med 23(1):37–45CrossRefGoogle Scholar
  16. Detre JA, Wang J, Wang Z, Rao H (2009) Arterial spin-labeled perfusion MRI in basic and clinical neuroscience. Curr Opin Neurol 22(4):348–355PubMedCrossRefGoogle Scholar
  17. Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118(Pt 1):279–306PubMedCrossRefGoogle Scholar
  18. DeYoung CG, Hirsh JB, Shane MS, Papademetris X, Rajeevan N, Gray JR (2010) Testing predictions from personality neuroscience. Brain structure and the big five. Psychol Sci 21(6):820–828PubMedCentralPubMedCrossRefGoogle Scholar
  19. Eysenck HJ, Eysenck SBG (1991) Manual of the Eysenck Personality Scales. Hodder and Stoughton, LondonGoogle Scholar
  20. Farde L, Gustavsson JP, Jonsson E (1997) D2 dopamine receptors and personality traits. Nature 385(6617):590PubMedCrossRefGoogle Scholar
  21. Farmer AD, Shwahdi M, Kano M, Rossiter H, Kishor J, Worthen SF, Coen SJ, Aziz Q (2009) Neuroticism predicts autonomic nervous system responses to visceral pain. Gastroenterology 136(5):A725–A725CrossRefGoogle Scholar
  22. Friedman BH (2007) An autonomic flexibility-neurovisceral integration model of anxiety and cardiac vagal tone. Biol Psychol 74(2):185–199PubMedCrossRefGoogle Scholar
  23. Gianaros PJ, Van Der Veen FM, Jennings JR (2004) Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: implications for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology 41(4):521–530PubMedCrossRefGoogle Scholar
  24. Haas BW, Omura K, Constable RT, Canli T (2007) Emotional conflict and neuroticism: personality-dependent activation in the amygdala and subgenual anterior cingulate. Behav Neurosci 121(2):249–256PubMedCrossRefGoogle Scholar
  25. Haier RJ (1987) The study of personality with positron emission tomography. Personality dimensions and arousal. Plenum Press, New YorkGoogle Scholar
  26. Hariri AR (2009) The neurobiology of individual differences in complex behavioral traits. Annu Rev Neurosci 32:225–247PubMedCentralPubMedCrossRefGoogle Scholar
  27. Jimura K, Konishi S, Miyashita Y (2009) Temporal pole activity during perception of sad faces, but not happy faces, correlates with neuroticism trait. Neurosci Lett 453(1):45–48PubMedCrossRefGoogle Scholar
  28. Jimura K, Konishi S, Asari T, Miyashita Y (2010) Temporal pole activity during understanding other persons’ mental states correlates with neuroticism trait. Brain Res 1328:104–112PubMedCrossRefGoogle Scholar
  29. Julu PO (1992) A linear scale for measuring vagal tone in man. J Auton Pharmacol 12(2):109–115PubMedCrossRefGoogle Scholar
  30. Kim SH, Hwang JH, Park HS, Kim SE (2008) Resting brain metabolic correlates of neuroticism and extraversion in young men. Neuroreport 19(8):883–886PubMedCrossRefGoogle Scholar
  31. Kumari V, ffytche DH, Williams SC, Gray JA (2004) Personality predicts brain responses to cognitive demands. J Neurosci 24(47):10636–10641PubMedCrossRefGoogle Scholar
  32. Kunisato Y, Okamoto Y, Okada G, Aoyama S, Nishiyama Y, Onoda K, Yamawaki S (2011) Personality traits and the amplitude of spontaneous low-frequency oscillations during resting state. Neurosci Lett 492(2):109–113PubMedCrossRefGoogle Scholar
  33. Lane RD, Wager TD (2009a) Introduction to a special issue of Neuroimage on brain-body medicine. Neuroimage 47(3):781–784PubMedCrossRefGoogle Scholar
  34. Lane RD, Wager TD (2009b) The new field of brain-body medicine: what have we learned and where are we headed? Neuroimage 47(3):1135–1140PubMedCrossRefGoogle Scholar
  35. Lane RD, McRae K, Reiman EM, Chen K, Ahern GL, Thayer JF (2009) Neural correlates of heart rate variability during emotion. Neuroimage 44(1):213–222PubMedCrossRefGoogle Scholar
  36. Maschke M (2002) Fear conditioned changes of heart rate in patients with medial cerebellar lesions. J Neurol Neurosurg Psychiatry 72(1):116–118. doi: 10.1136/jnnp.72.1.116 PubMedCentralPubMedCrossRefGoogle Scholar
  37. Medford N, Critchley HD (2010) Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response. Brain Struct Funct 214(5–6):535–549PubMedCentralPubMedCrossRefGoogle Scholar
  38. Ming X, Julu PO, Brimacombe M, Connor S, Daniels ML (2005) Reduced cardiac parasympathetic activity in children with autism. Brain Dev 27(7):509–516PubMedCrossRefGoogle Scholar
  39. Miu AC, Heilman RM, Miclea M (2009) Reduced heart rate variability and vagal tone in anxiety: trait versus state, and the effects of autogenic training. Auton Neuroscience Basic Clin 145(1–2):99–103CrossRefGoogle Scholar
  40. Nagai Y, Critchley HD, Featherstone E, Fenwick PB, Trimble MR, Dolan RJ (2004) Brain activity relating to the contingent negative variation: an fMRI investigation. Neuroimage 21(4):1232–1241PubMedCrossRefGoogle Scholar
  41. O’Gorman RL, Kumari V, Williams SC, Zelaya FO, Connor SE, Alsop DC, Gray JA (2006) Personality factors correlate with regional cerebral perfusion. Neuroimage 31(2):489–495PubMedCrossRefGoogle Scholar
  42. Paine P, Kishor J, Worthen SF, Gregory LJ, Aziz Q (2009a) Exploring relationships for visceral and somatic pain with autonomic control and personality. Pain 144(3):236–244PubMedCrossRefGoogle Scholar
  43. Paine P, Worthen SF, Gregory LJ, Thompson DG, Aziz Q (2009b) Personality differences affect brainstem autonomic responses to visceral pain. Neurogastroenterol Motil 21(11):e1155–e1198CrossRefGoogle Scholar
  44. Parkes LM, Rashid W, Chard DT, Tofts PS (2004) Normal cerebral perfusion measurements using arterial spin labeling: reproducibility, stability, and age and gender effects. Magn Reson Med 51(4):736–743PubMedCrossRefGoogle Scholar
  45. Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2(6):417–424PubMedCrossRefGoogle Scholar
  46. Rhodes RA, Murthy NV, Dresner MA, Selvaraj S, Stavrakakis N, Babar S, Cowen PJ, Grasby PM (2007) Human 5-HT transporter availability predicts amygdala reactivity in vivo. J Neurosci 27(34):9233–9237PubMedCrossRefGoogle Scholar
  47. Rottenberg J, Clift A, Bolden S, Salomon K (2007) RSA fluctuation in major depressive disorder. Psychophysiology 44(3):450–458PubMedCrossRefGoogle Scholar
  48. Sack M, Hopper JW, Lamprecht F (2004) Low respiratory sinus arrhythmia and prolonged psychophysiological arousal in posttraumatic stress disorder: heart rate dynamics and individual differences in arousal regulation. Biol Psychiatry 55(3):284–290PubMedCrossRefGoogle Scholar
  49. Sadikot AF, Parent A (1990) The monoaminergic innervation of the amygdala in the squirrel monkey: an immunohistochemical study. Neuroscience 36(2):431–447PubMedCrossRefGoogle Scholar
  50. Sebastiani L, La Noce A, Paton JF, Ghelarducci B (1992) Influence of the cerebellar posterior vermis on the acquisition of the classically conditioned bradycardic response in the rabbit. Exp Brain Res 88(1):193–198PubMedCrossRefGoogle Scholar
  51. Stahl J, Rammsayer T (2008) Extroversion-related differences in speed of premotor and motor processing as revealed by lateralized readiness potentials. J Mot Behav 40(2):143–154PubMedCrossRefGoogle Scholar
  52. Suckling J, Bullmore E (2004) Permutation tests for factorially designed neuroimaging experiments. Hum Brain Mapp 22(3):193–205PubMedCrossRefGoogle Scholar
  53. Suzuki H, Watanabe S, Hamaguchi T, Mine H, Terui T, Kanazawa M, Oohisa N, Maruyama M, Yambe T, Itoh M, Fukudo S (2009) Brain activation associated with changes in heart rate, heart rate variability, and plasma catecholamines during rectal distention. Psychosom Med 71(6):619–626PubMedCrossRefGoogle Scholar
  54. Task Force of The European Society of Cardiology and The North American Society of Pacing and Electrophysiology (1996) Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Eur Heart J.17(3):354–381Google Scholar
  55. Ter Horst GJ, Hautvast RW, De Jongste MJ, Korf J (1996) Neuroanatomy of cardiac activity-regulating circuitry: a transneuronal retrograde viral labelling study in the rat. Eur J Neurosci 8(10):2029–2041PubMedCrossRefGoogle Scholar
  56. Thayer JF, Lane RD (2007) The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychol 74(2):224–242PubMedCrossRefGoogle Scholar
  57. Thayer JF, Lane RD (2009) Claude Bernard and the heart–brain connection: further elaboration of a model of neurovisceral integration. Neurosci Biobehav Rev 33(2):81–88PubMedCrossRefGoogle Scholar
  58. Tjandra T, Brooks JC, Figueiredo P, Wise R, Matthews PM, Tracey I (2005) Quantitative assessment of the reproducibility of functional activation measured with BOLD and MR perfusion imaging: implications for clinical trial design. Neuroimage 27(2):393–401PubMedCrossRefGoogle Scholar
  59. Wager TD, Waugh CE, Lindquist M, Noll DC, Fredrickson BL, Taylor SF (2009) Brain mediators of cardiovascular responses to social threat: part I: reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. Neuroimage 47(3):821–835PubMedCentralPubMedCrossRefGoogle Scholar
  60. Wang J, Rao H, Wetmore GS, Furlan PM, Korczykowski M, Dinges DF, Detre JA (2005) Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. Proc Natl Acad Sci USA 102(49):17804–17809PubMedCentralPubMedCrossRefGoogle Scholar
  61. Wolf RL, Detre JA (2007) Clinical neuroimaging using arterial spin-labeled perfusion magnetic resonance imaging. Neurotherapeutics 4(3):346–359PubMedCentralPubMedCrossRefGoogle Scholar
  62. Wright CI, Williams D, Feczko E, Barrett LF, Dickerson BC, Schwartz CE, Wedig MM (2006) Neuroanatomical correlates of extraversion and neuroticism. Cereb Cortex 16(12):1809–1819PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • M. Kano
    • 1
    • 2
  • S. J. Coen
    • 1
    • 3
  • A. D. Farmer
    • 1
  • Q. Aziz
    • 1
  • S. C. R. Williams
    • 3
  • D. C. Alsop
    • 4
  • S. Fukudo
    • 2
  • R. L. O’Gorman
    • 3
    • 5
    • 6
    Email author
  1. 1.Centre for Digestive Diseases, Wingate Institute of Neurogastroenterology, Blizard Institute of Cell and Molecular ScienceBarts and the London School of Medicine and Dentistry, Queen Mary College, University of LondonLondonUK
  2. 2.Behavioral MedicineTohoku University Graduate School of MedicineSendaiJapan
  3. 3.Centre for Neuroimaging SciencesKing’s College London Institute of PsychiatryLondonUK
  4. 4.Department of RadiologyBeth Israel Deaconess Medical Center, Harvard Medical SchoolBostonUSA
  5. 5.Center for Magnetic Resonance ResearchUniversity Children’s HospitalZurichSwitzerland
  6. 6.Center for Integrative Human PhysiologyZurichSwitzerland

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