Brain Topography

, Volume 31, Issue 3, pp 477–487 | Cite as

Intrinsic Network Connectivity Patterns Underlying Specific Dimensions of Impulsiveness in Healthy Young Adults

  • Katharina M. Kubera
  • Dusan Hirjak
  • Nadine D. Wolf
  • Fabio Sambataro
  • Philipp A. Thomann
  • R. Christian Wolf
Original Paper


Impulsiveness is a central human personality trait and of high relevance for the development of several mental disorders. Impulsiveness is a multidimensional construct, yet little is known about dimension-specific neural correlates. Here, we address the question whether motor, attentional and non-planning components, as measured by the Barratt Impulsiveness Scale (BIS-11), are associated with distinct or overlapping neural network activity. In this study, we investigated brain activity at rest and its relationship to distinct dimensions of impulsiveness in 30 healthy young adults (m/f = 13/17; age mean/SD = 26.4/2.6 years) using resting-state functional magnetic resonance imaging at 3T. A spatial independent component analysis and a multivariate model selection strategy were used to identify systems loading on distinct impulsivity domains. We first identified eight networks for which we had a-priori hypotheses. These networks included basal ganglia, cortical motor, cingulate and lateral prefrontal systems. From the eight networks, three were associated with impulsiveness measures (p < 0.05, FDR corrected). There were significant relationships between right frontoparietal network function and all three BIS domains. Striatal and midcingulate network activity was associated with motor impulsiveness only. Within the networks regionally confined effects of age and gender were found. These data suggest distinct and overlapping patterns of neural activity underlying specific dimensions of impulsiveness. Motor impulsiveness appears to be specifically related to striatal and midcingulate network activity, in contrast to a domain-unspecific right frontoparietal system. Effects of age and gender have to be considered in young healthy samples.


fMRI Resting-state Functional connectivity Impulsivity Barratt Impulsiveness Scale BIS 



We are grateful to all the participants and their families for their time and interest in this study.


This research received no specific grant from any funding agency, commercial or not-for-profit sectors.

Compliance with Ethical Standards

Conflict of interest

The authors have declared that there are no conflicts of interest in relation to the subject of this study.

Ethical Approval

The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008.

Supplementary material

10548_2017_604_MOESM1_ESM.doc (57 kb)
Supplementary material 1 (DOC 57 KB)
10548_2017_604_MOESM2_ESM.tif (13.1 mb)
Supplementary Figure 1. Spatiotemporal patterns of eight resting-state networks chosen for further multivariate analyses to investigate neural systems loadings on distinct domains of impulsiveness, as provided by the BIS-11 scale. The figures displays independent components (ICs) and their corresponding time courses, as identified by the group ICA. The color bars indicate Z-values, IC’s are thresholded above Z = 3.5. (TIF 13463 KB)
10548_2017_604_MOESM3_ESM.tif (103 kb)
Supplementary Figure 2. Univariate tests showing regional effects of age and gender over all resting-state networks, displayed as −sign(t)log10(p). Stereotaxic coordinates and Z-scores are provided in Table 1, supplementary data. Effects were considered significant at p &#x003C; 0.01, uncorrected. The panels show bar plots of average beta-values for age and gender terms, respectively. Beta-values were averaged over significant clusters showing the same directionality. The color of the bar is proportional to the fraction of voxels within components that contribute to each of the effects. (TIF 102 KB)


  1. Achterberg M et al (2016) Control your anger! The neural basis of aggression regulation in response to negative social feedback. Soc Cogn Affect Neurosci 11:712–720CrossRefPubMedPubMedCentralGoogle Scholar
  2. Adinoff B et al (2006) Sex differences in medial and lateral orbitofrontal cortex hypoperfusion in cocaine-dependent men and women. Gend Med 3:206–222CrossRefPubMedPubMedCentralGoogle Scholar
  3. Aichert DS et al (2012) Associations between trait impulsivity and prepotent response inhibition. J Clin Exp Neuropsychol 34:1016–1032CrossRefPubMedGoogle Scholar
  4. Allen EA et al (2011) A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci 5:2PubMedPubMedCentralGoogle Scholar
  5. Aron AR (2011) From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biol Psychiatry 69:e55–e68CrossRefPubMedGoogle Scholar
  6. Aron AR, Poldrack RA (2005) The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder. Biol Psychiatry 57:1285–1292CrossRefPubMedGoogle Scholar
  7. Aron AR, Poldrack RA (2006) Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J Neurosci 26:2424–2433CrossRefPubMedGoogle Scholar
  8. Aron AR et al (2003) Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6:115–116CrossRefPubMedGoogle Scholar
  9. Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177CrossRefPubMedGoogle Scholar
  10. Asahi S et al (2004) Negative correlation between right prefrontal activity during response inhibition and impulsiveness: a fMRI study. Eur Arch Psychiatry Clin Neurosci 254:245–251CrossRefPubMedGoogle Scholar
  11. Bari A, Robbins TW (2013) Inhibition and impulsivity: behavioral and neural basis of response control. Prog Neurobiol 108:44–79CrossRefPubMedGoogle Scholar
  12. Bernstein GA et al (2016) Abnormal striatal resting-state functional connectivity in adolescents with obsessive-compulsive disorder. Psychiatry Res 247:49–56CrossRefPubMedGoogle Scholar
  13. Biswal BB et al (2010) Toward discovery science of human brain function. Proc Natl Acad Sci USA 107:4734–4739CrossRefPubMedPubMedCentralGoogle Scholar
  14. Blakemore SJ, Robbins TW (2012) Decision-making in the adolescent brain. Nat Neurosci 15:1184–1191CrossRefPubMedGoogle Scholar
  15. Boehler CN et al (2012) Motivating inhibition—reward prospect speeds up response cancellation. Cognition 125:498–503CrossRefPubMedGoogle Scholar
  16. Brown MR et al (2015a) fMRI investigation of response inhibition, emotion, impulsivity, and clinical high-risk behavior in adolescents. Front Syst Neurosci 9:124PubMedPubMedCentralGoogle Scholar
  17. Brown MR et al (2015b) Neural correlates of high-risk behavior tendencies and impulsivity in an emotional Go/NoGo fMRI task. Front Syst Neurosci 9:24PubMedPubMedCentralGoogle Scholar
  18. Chamberlain SR et al (2007) Impaired cognitive flexibility and motor inhibition in unaffected first-degree relatives of patients with obsessive-compulsive disorder. Am J Psychiatry 164:335–338CrossRefPubMedPubMedCentralGoogle Scholar
  19. Chambers RA, Potenza MN (2003) Neurodevelopment, impulsivity, and adolescent gambling. J Gambl Stud 19:53–84CrossRefPubMedGoogle Scholar
  20. Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215CrossRefPubMedGoogle Scholar
  21. Correa N et al (2005) Comparison of blind source separation algorithms for FMRI using a new Matlab toolbox: GIFT. Proc IEEE Int Conf Acoust Speech Signal Process 5:401–404Google Scholar
  22. Cuthbert BN, Insel TR (2013) Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Med 11:126CrossRefPubMedPubMedCentralGoogle Scholar
  23. Cyders MA, Coskunpinar A (2011) Measurement of constructs using self-report and behavioral lab tasks: is there overlap in nomothetic span and construct representation for impulsivity? Clin Psychol Rev 31:965–982CrossRefPubMedGoogle Scholar
  24. Davis FC et al (2013) Impulsivity and the modular organization of resting-state neural networks. Cereb Cortex 23:1444–1452CrossRefPubMedGoogle Scholar
  25. de Wit SJ et al (2012) Presupplementary motor area hyperactivity during response inhibition: a candidate endophenotype of obsessive-compulsive disorder. Am J Psychiatry 169:1100–1108CrossRefPubMedGoogle Scholar
  26. Delgado MR, Gillis MM, Phelps EA (2008) Regulating the expectation of reward via cognitive strategies. Nat Neurosci 11:880–881CrossRefPubMedPubMedCentralGoogle Scholar
  27. Eysenck SB, Eysenck HJ (1978) Impulsiveness and venturesomeness: their position in a dimensional system of personality description. Psychol Rep 43:1247–1255CrossRefPubMedGoogle Scholar
  28. Farr OM et al (2012) Decreased saliency processing as a neural measure of Barratt impulsivity in healthy adults. Neuroimage 63:1070–1077CrossRefPubMedPubMedCentralGoogle Scholar
  29. Fassbender C et al (2004) A topography of executive functions and their interactions revealed by functional magnetic resonance imaging. Brain Res Cogn Brain Res 20:132–143CrossRefPubMedGoogle Scholar
  30. Fineberg NA et al (2014) New developments in human neurocognition: clinical, genetic, and brain imaging correlates of impulsivity and compulsivity. CNS Spectr 19:69–89CrossRefPubMedPubMedCentralGoogle Scholar
  31. Fuster J (2008) The prefrontal cortex. Academic Press, LondonGoogle Scholar
  32. Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12:652–669CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hariri AR et al (2006) Preference for immediate over delayed rewards is associated with magnitude of ventral striatal activity. J Neurosci 26:13213–13217CrossRefPubMedGoogle Scholar
  34. Hester R, Fassbender C, Garavan H (2004) Individual differences in error processing: a review and reanalysis of three event-related fMRI studies using the GO/NOGO task. Cereb Cortex 14:986–994CrossRefPubMedGoogle Scholar
  35. Himberg J, Hyvarinen A, Esposito F (2004) Validating the independent components of neuroimaging time series via clustering and visualization. Neuroimage 22:1214–1222CrossRefPubMedGoogle Scholar
  36. Hirjak D et al (2016) Cortical folding patterns are associated with impulsivity in healthy young adults. Brain Imaging Behav.
  37. Horn NR et al (2003) Response inhibition and impulsivity: an fMRI study. Neuropsychologia 41:1959–1966CrossRefPubMedGoogle Scholar
  38. Kim S, Lee D (2011) Prefrontal cortex and impulsive decision making. Biol Psychiatry 69:1140–1146CrossRefPubMedGoogle Scholar
  39. Kirby KN (2009) One-year temporal stability of delay-discount rates. Psychon Bull Rev 16:457–462CrossRefPubMedGoogle Scholar
  40. Knutson B et al (2001) Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport 12:3683–3687CrossRefPubMedGoogle Scholar
  41. Konishi S et al (1999) Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain 122(Pt 5):981–991CrossRefPubMedGoogle Scholar
  42. Laird AR et al (2011) Behavioral interpretations of intrinsic connectivity networks. J Cognitive Neurosci 23(12):4022–4037CrossRefGoogle Scholar
  43. Lei D et al (2015) Functional MRI reveals different response inhibition between adults and children with ADHD. Neuropsychology 29:874–881CrossRefPubMedGoogle Scholar
  44. Levy R, Goldman-Rakic PS (2000) Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133:23–32CrossRefPubMedGoogle Scholar
  45. Li YO, Adali T, Calhoun VD (2007) Estimating the number of independent components for functional magnetic resonance imaging data. Hum Brain Mapp 28:1251–1266CrossRefPubMedGoogle Scholar
  46. Li N et al (2013) Resting-state functional connectivity predicts impulsivity in economic decision-making. J Neurosci 33:4886–4895CrossRefPubMedGoogle Scholar
  47. Lijffijt M et al (2004) Differences between low and high trait impulsivity are not associated with differences in inhibitory motor control. J Atten Disord 8:25–32CrossRefPubMedGoogle Scholar
  48. Liu J, Zubieta JK, Heitzeg M (2012) Sex differences in anterior cingulate cortex activation during impulse inhibition and behavioral correlates. Psychiatry Res 201:54–62CrossRefPubMedPubMedCentralGoogle Scholar
  49. Logan TF et al (1997) Biologic response modulation by tumor necrosis factor alpha (TNF alpha) in a phase Ib trial in cancer patients. J Immunother 20:387–398CrossRefPubMedGoogle Scholar
  50. Matsuo K et al (2009) A voxel-based morphometry study of frontal gray matter correlates of impulsivity. Hum Brain Mapp 30:1188–1195CrossRefPubMedGoogle Scholar
  51. McClure SM et al (2004) Separate neural systems value immediate and delayed monetary rewards. Science 306:503–507CrossRefPubMedGoogle Scholar
  52. Meyer-Lindenberg A et al (2006) Neural mechanisms of genetic risk for impulsivity and violence in humans. Proc Natl Acad Sci USA 103:6269–6274CrossRefPubMedPubMedCentralGoogle Scholar
  53. Milad MR, Rauch SL (2012) Obsessive-compulsive disorder: beyond segregated cortico-striatal pathways. Trends Cogn Sci 16:43–51CrossRefPubMedGoogle Scholar
  54. Milad MR et al (2013) Deficits in conditioned fear extinction in obsessive-compulsive disorder and neurobiological changes in the fear circuit. JAMA Psychiatry 70:608–618 (quiz 554)CrossRefPubMedGoogle Scholar
  55. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202CrossRefPubMedGoogle Scholar
  56. Moeller FG et al (2001) Psychiatric aspects of impulsivity. Am J Psychiatry 158:1783–1793CrossRefPubMedGoogle Scholar
  57. Nambu A, Tokuno H, Takada M (2002) Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci Res 43:111–117CrossRefPubMedGoogle Scholar
  58. Oldehinkel M et al (2016) Attention-deficit/hyperactivity disorder symptoms coincide with altered striatal connectivity. Biol Psychiatry 1:353–363Google Scholar
  59. Paus T et al (1993) Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. J Neurophysiol 70:453–469CrossRefPubMedGoogle Scholar
  60. Peters J, Buchel C (2011) The neural mechanisms of inter-temporal decision-making: understanding variability. Trends Cogn Sci 15:227–239CrossRefPubMedGoogle Scholar
  61. Pietrini P et al (2000) Neural correlates of imaginal aggressive behavior assessed by positron emission tomography in healthy subjects. Am J Psychiatry 157:1772–1781CrossRefPubMedGoogle Scholar
  62. Plichta MM, Scheres A (2014) Ventral-striatal responsiveness during reward anticipation in ADHD and its relation to trait impulsivity in the healthy population: a meta-analytic review of the fMRI literature. Neurosci Biobehav Rev 38:125–134CrossRefPubMedGoogle Scholar
  63. Posner J, Park C, Wang Z (2014) Connecting the dots: a review of resting connectivity MRI studies in attention-deficit/hyperactivity disorder. Neuropsychol Rev 24:3–15CrossRefPubMedPubMedCentralGoogle Scholar
  64. Power JD et al (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154CrossRefPubMedGoogle Scholar
  65. Rubia K et al (2001) Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage 13:250–261CrossRefPubMedGoogle Scholar
  66. Schilling C et al (2013) Cortical thickness of superior frontal cortex predicts impulsiveness and perceptual reasoning in adolescence. Mol Psychiatry 18:624–630CrossRefPubMedGoogle Scholar
  67. Schmaal L et al (2012) The association between cingulate cortex glutamate concentration and delay discounting is mediated by resting state functional connectivity. Brain Behav 2:553–562CrossRefPubMedPubMedCentralGoogle Scholar
  68. Smith SM et al (2009) Correspondence of the brain’s functional architecture during activation and rest. P Natl Acad Sci 106(31):13040–13045CrossRefGoogle Scholar
  69. Stanford MS et al (2009) Fifty years of the Barratt Impulsiveness Scale: an update and review. Personality Individ Differ 47:385–395CrossRefGoogle Scholar
  70. Stein DJ, Hollander E (1995) Obsessive-compulsive spectrum disorders. J Clin Psychiatry 56:265–266PubMedGoogle Scholar
  71. Stoltenberg SF (2008) Does gender moderate associations among impulsivity and health-risk behaviors? Addict Behav 33(2):252–265CrossRefPubMedGoogle Scholar
  72. Tschernegg M et al (2015) Impulsivity relates to striatal gray matter volumes in humans: evidence from a delay discounting paradigm. Front Hum Neurosci 9:384CrossRefPubMedPubMedCentralGoogle Scholar
  73. 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 15:273–289CrossRefPubMedGoogle Scholar
  74. Urcelay GP, Dalley JW (2012) Linking ADHD, impulsivity, and drug abuse: a neuropsychological perspective. Curr Top Behav Neurosci 9:173–197CrossRefPubMedGoogle Scholar
  75. Whelan R et al (2012) Adolescent impulsivity phenotypes characterized by distinct brain networks. Nat Neurosci 15:920–925CrossRefPubMedGoogle Scholar
  76. Wilbertz T et al (2014) Response inhibition and its relation to multidimensional impulsivity. Neuroimage 103:241–248CrossRefPubMedGoogle Scholar
  77. Yip SW, Potenza MN (2016) Application of research domain criteria to childhood and adolescent impulsive and addictive disorders: implications for treatment. Clin Psychol Rev.

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Katharina M. Kubera
    • 1
  • Dusan Hirjak
    • 2
  • Nadine D. Wolf
    • 1
  • Fabio Sambataro
    • 3
  • Philipp A. Thomann
    • 1
    • 4
  • R. Christian Wolf
    • 1
  1. 1.Department of General Psychiatry, Center for Psychosocial MedicineUniversity of HeidelbergHeidelbergGermany
  2. 2.Department of Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty MannheimHeidelberg UniversityMannheimGermany
  3. 3.Department of Experimental and Clinical Medical Sciences (DISM)University of UdineUdineItaly
  4. 4.Center for Mental Health, Odenwald District Healthcare CenterErbachGermany

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