Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Default network and frontoparietal control network theta connectivity supports internal attention

Abstract

Attending to our inner world is a fundamental cognitive phenomenon1,2,3, yet its neural underpinnings remain largely unknown. Neuroimaging evidence implicates the default network (DN) and frontoparietal control network (FPCN)4; however, the electrophysiological basis for the interaction between these networks is unclear. Here we recorded intracranial electroencephalogram from DN and FPCN electrodes implanted in individuals undergoing presurgical monitoring for refractory epilepsy. Subjects performed an attention task during which they attended to tones (that is, externally directed attention) or ignored the tones and thought about whatever came to mind (that is, internally directed attention). Given the emerging role of theta band connectivity in attentional processes5,6, we examined the theta power correlation between DN and two subsystems of the FPCN as a function of attention states. We found increased connectivity between DN and FPCNA during internally directed attention compared to externally directed attention, which positively correlated with attention ratings. There was no statistically significant difference between attention states in the connectivity between DN and FPCNB. Our results indicate that enhanced theta band connectivity between the DN and FPCNA is a core electrophysiological mechanism that underlies internally directed attention.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Experimental task and electrode coverage.
Fig. 2: Theta band connectivity between DN and FPCN subsystems.
Fig. 3: Connectivity between DN and FPCN subsystems across the low-frequency range; and their correlations with attention ratings.

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon request.

Code availability

The custom MATLAB code used to analyse the data that support the findings of this study are available from the corresponding author upon request.

References

  1. Christoff, K., Irving, Z. C., Fox, K. C. R., Spreng, R. N. & Andrews-Hanna, J. R. Mind-wandering as spontaneous thought: a dynamic framework. Nat. Rev. Neurosci. 17, 718–731 (2016).

    CAS  PubMed  Google Scholar 

  2. Smallwood, J. & Schooler, J. W. The restless mind. Psychol. Bull. 132, 946–958 (2006).

    PubMed  Google Scholar 

  3. Mittner, M., Hawkins, G. E., Boekel, W. & Forstmann, B. U. A neural model of mind wandering. Trends Cogn. Sci. 20, 570–578 (2016).

    PubMed  Google Scholar 

  4. Dixon, M. L. et al. Heterogeneity within the frontoparietal control network and its relationship to the default and dorsal attention networks. Proc. Natl Acad. Sci. USA 115, E1598–E1607 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Baird, B., Smallwood, J., Lutz, A. & Schooler, J. W. The decoupled mind: mind-wandering disrupts cortical phase-locking to perceptual events. J. Cogn. Neurosci. 26, 2596–2607 (2014).

    PubMed  Google Scholar 

  6. Helfrich, R. F. et al. Neural mechanisms of sustained attention are rhythmic. Neuron 99, 854–865 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Killingsworth, M. A. & Gilbert, D. T. A wandering mind is an unhappy mind. Science 330, 932 (2010).

    CAS  PubMed  Google Scholar 

  8. Foster, B. L., Rangarajan, V., Shirer, W. R. & Parvizi, J. Intrinsic and task-dependent coupling of neuronal population activity in human parietal cortex. Neuron 86, 578–590 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Sormaz, M. et al. Default mode network can support the level of detail in experience during active task states. Proc. Natl Acad. Sci. USA 115, 9318–9323 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Zabelina, D. L. & Andrews-Hanna, J. R. Dynamic network interactions supporting internally-oriented cognition. Curr. Opin. Neurobiol. 40, 86–93 (2016).

    CAS  PubMed  Google Scholar 

  11. Fox, K. C. R., Spreng, R. N., Ellamil, M., Andrews-Hanna, J. R. & Christoff, K. The wandering brain: meta-analysis of functional neuroimaging studies of mind-wandering and related spontaneous thought processes. Neuroimage 111, 611–621 (2015).

    PubMed  Google Scholar 

  12. Mason, M. F. et al. Wandering minds: the default network and stimulus-independent thought. Science 315, 393–395 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Margulies, D. S. et al. Situating the default-mode network along a principal gradient of macroscale cortical organization. Proc. Natl Acad. Sci. USA 113, 12574–12579 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Buckner, R. L., Andrews-Hanna, J. R. & Schacter, D. L. The brain’s default network: anatomy, function, and relevance to disease. Ann. NY Acad. Sci. 1124, 1–38 (2008).

    PubMed  Google Scholar 

  15. Raichle, M. E. The brain’s default mode network. Annu. Rev. Neurosci. 38, 433–447 (2015).

    CAS  PubMed  Google Scholar 

  16. Schacter, D. L., Addis, D. R. & Buckner, R. L. Remembering the past to imagine the future: the prospective brain. Nat. Rev. Neurosci. 8, 657–661 (2007).

    CAS  PubMed  Google Scholar 

  17. Kam, J. W. Y., Solbakk, A. K., Endestad, T., Meling, T. R. & Knight, R. T. Lateral prefrontal cortex lesion impairs regulation of internally and externally directed attention. Neuroimage 175, 91–99 (2018).

    PubMed  Google Scholar 

  18. Spreng, R. N., Stevens, W. D., Chamberlain, J. P., Gilmore, A. W. & Schacter, D. L. Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition. Neuroimage 53, 303–317 (2010).

    PubMed  Google Scholar 

  19. Dodds, C. M., Morein-Zamir, S. & Robbins, T. W. Dissociating inhibition, attention, and response control in the frontoparietal network using functional magnetic resonance imaging. Cereb. Cortex 21, 1155–1165 (2011).

    PubMed  Google Scholar 

  20. Yeo, B. T. T. et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106, 1125–1165 (2011).

    PubMed  Google Scholar 

  21. Engel, A. K., Gerloff, C., Hilgetag, C. C. & Nolte, G. Intrinsic coupling modes: multiscale interactions in ongoing brain activity. Neuron 80, 867–886 (2013).

    CAS  PubMed  Google Scholar 

  22. Siegel, M., Donner, T. H. & Engel, A. K. Spectral fingerprints of large-scale neuronal interactions. Nat. Rev. Neurosci. 13, 121–134 (2012).

    CAS  PubMed  Google Scholar 

  23. Foster, B. L., Kaveh, A., Dastjerdi, M., Miller, K. J. & Parvizi, J. Human retrosplenial cortex displays transient theta phase locking with medial temporal cortex prior to activation during autobiographical memory retrieval. J. Neurosci. 33, 10439–10446 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Hipp, J. F. & Siegel, M. BOLD fMRI correlation reflects frequency-specific neuronal correlation. Curr. Biol. 25, 1368–1374 (2015).

    CAS  PubMed  Google Scholar 

  25. Cooper, P. S. et al. Theta frontoparietal connectivity associated with proactive and reactive cognitive control processes. Neuroimage 108, 354–363 (2015).

    PubMed  Google Scholar 

  26. Fellrath, J., Mottaz, A., Schnider, A., Guggisberg, A. G. & Ptak, R. Theta-band functional connectivity in the dorsal fronto-parietal network predicts goal-directed attention. Neuropsychologia 92, 20–30 (2016).

    PubMed  Google Scholar 

  27. Andrews-Hanna, J. R., Reidler, J. S., Sepulcre, J., Poulin, R. & Buckner, R. L. Functional-anatomic fractionation of the brain’s default network. Neuron 65, 550–562 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Mittner, M. et al. When the brain takes a break: a model-based analysis of mind wandering. J. Neurosci. 34, 16286–16295 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Smallwood, J. et al. Pupillometric evidence for the decoupling of attention from perceptual input during offline thought. PLoS One 6, e18298 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Colclough, G. L. et al. How reliable are MEG resting-state connectivity metrics? Neuroimage 138, 284–293 (2016).

    CAS  PubMed  Google Scholar 

  31. Baayen, R. H., Davidson, D. J. & Bates, D. M. Mixed-effects modeling with crossed random effects for subjects and items. J. Mem. Lang. 59, 390–412 (2008).

    Google Scholar 

  32. Jensen, O. & Mazaheri, A. Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front. Hum. Neurosci. 4, 186 (2010).

    PubMed  PubMed Central  Google Scholar 

  33. Gao, W. & Lin, W. Frontal parietal control network regulates the anti-correlated default and dorsal attention networks. Hum. Brain Mapp. 33, 192–202 (2012).

    PubMed  Google Scholar 

  34. Clayton, M. S., Yeung, N. & Cohen Kadosh, R. The roles of cortical oscillations in sustained attention. Trends Cogn. Sci. 19, 188–195 (2015).

    PubMed  Google Scholar 

  35. Sauseng, P., Hoppe, J., Klimesch, W., Gerloff, C. & Hummel, F. C. Dissociation of sustained attention from central executive functions: local activity and interregional connectivity in the theta range. Eur. J. Neurosci. 25, 587–593 (2007).

    CAS  PubMed  Google Scholar 

  36. Jensen, O. & Tesche, C. D. Frontal theta activity in humans increases with memory load in a working memory task. Eur. J. Neurosci. 15, 1395–1399 (2002).

    PubMed  Google Scholar 

  37. Tesche, C. D. & Karhu, J. MEG study of hippocampal theta during a working memory task. Biomed. Tech. 44, 74–78 (1999).

    Google Scholar 

  38. Brovelli, A. et al. Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. Proc. Natl Acad. Sci. USA 101, 9849–9854 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Elton, A. & Gao, W. Divergent task-dependent functional connectivity of executive control and salience networks. Cortex 51, 56–66 (2014).

    PubMed  Google Scholar 

  40. Noonan, K., Jefferies, E., Visser, M. & Ralph, M. A. L. Going beyond inferior prefrontal involvement in semantic control: evidence for the additional contribution of dorsal angular gyrus and posterior middle temporal cortex. J. Cogn. Neurosci. 25, 1824–1850 (2013).

    PubMed  Google Scholar 

  41. Christoff, K., Keramatian, K., Gordon, A., Smith, R. & Mädler, B. Prefrontal organization of cognitive control according to levels of abstraction. Brain Res. 1286, 94–105 (2009).

    CAS  PubMed  Google Scholar 

  42. Bhatt, M., Lohrenz, T., Camerer, C. & Montague, P. Neural signatures of strategic types in a two-person bargaining game. Proc. Natl Acad. Sci. USA 107, 19720–19725 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Addis, D. R., Wong, A. T. & Schacter, D. L. Remembering the past and imagining the future: common and distinct neural substrates during event construction and elaboration. Neuropsychologia 45, 1363–1377 (2007).

    PubMed  Google Scholar 

  44. Turnbull, A. et al. The ebb and flow of attention: between-subject variation in intrinsic connectivity and cognition associated with the dynamics of ongoing experience. Neuroimage 185, 286–299 (2019).

    PubMed  Google Scholar 

  45. Murphy, C. et al. Distant from input: evidence of regions within the default mode network supporting perceptually-decoupled and conceptually-guided cognition. Neuroimage 171, 393–401 (2018).

    PubMed  Google Scholar 

  46. Vatansever, D., Menon, D. K., Manktelow, A. E., Sahakian, B. J. & Stamatakis, E. A. Default mode dynamics for global functional integration. J. Neurosci. 35, 15254–15262 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Fox, M. D. et al. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl Acad. Sci. USA 102, 9673–9678 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Karapanagiotidis, T., Bernhardt, B. C., Jefferies, E. & Smallwood, J. Tracking thoughts: exploring the neural architecture of mental time travel during mind-wandering. Neuroimage 147, 272–281 (2017).

    PubMed  Google Scholar 

  49. Dixon, M. L., Fox, K. C. R. & Christoff, K. A framework for understanding the relationship between externally and internally directed cognition. Neuropsychologia 62, 321–330 (2014).

    PubMed  Google Scholar 

  50. Seli, P., Risko, E. F., Smilek, D. & Schacter, D. L. Mind-wandering with and without intention. Trends Cogn. Sci. 20, 605–617 (2016).

    PubMed  PubMed Central  Google Scholar 

  51. Stawarczyk, D., Majerus, S., Maj, M., Van der Linden, M. & D’Argembeau, A. Mind-wandering: phenomenology and function as assessed with a novel experience sampling method. Acta Psychol. 136, 370–381 (2011).

    Google Scholar 

  52. Jafarpour, A., Piai, V., Lin, J. J. & Knight, R. T. Human hippocampal pre-activation predicts behavior. Sci. Rep. 7, 5959 (2017).

    PubMed  PubMed Central  Google Scholar 

  53. Flinker, A. et al. Redefining the role of Broca’s area in speech. Proc. Natl Acad. Sci. USA 112, 2871–2875 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Johnson, E. L. et al. Dynamic frontotemporal systems process space and time in working memory. PLoS Biol. 16, e2004274 (2018).

    PubMed  PubMed Central  Google Scholar 

  55. Oostenveld, R., Fries, P., Maris, E. & Schoffelen, J. M. FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. 2011, 156869 (2011).

    PubMed  Google Scholar 

  56. Blenkmann, A. O. et al. iElectrodes: a comprehensive open-source toolbox for depth and subdural grid electrode localization. Front. Neuroinform. 11, 14 (2017).

    PubMed  PubMed Central  Google Scholar 

  57. Destrieux, C., Fischl, B., Dale, A. & Halgren, E. Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53, 1–15 (2010).

    PubMed  Google Scholar 

  58. Delorme, A. & Makeig, S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134, 9–21 (2004).

    PubMed  Google Scholar 

  59. Haller, M. et al. Persistent neuronal activity in human prefrontal cortex links perception and action. Nat. Hum. Behav. 2, 80–91 (2018).

    PubMed  Google Scholar 

  60. Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2014).

Download references

Acknowledgements

We appreciate the time put forward by our patients, whose participation was instrumental in this study. We thank A. Jafarpour, A. Breska, J. Zheng, R. Helfrich and V. Piai for discussions, as well as the recording team at each hospital for their help with data collection. This work was supported by the Natural Sciences and Engineering Research Council of Canada and the James S. McDonnell Foundation (to J.W.Y.K.), Research Council of Norway 240389/F20 and Internal Funding from the University of Oslo (to A.-K.S., T.E. and P.G.L.) and NINDS R3721135 (to R.T.K.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Contributions

J.W.Y.K. developed the research question and experimental design, analysed and interpreted the data and wrote the original draft of the manuscript. R.T.K. contributed to experimental design, data interpretation and revision of the manuscript. J.J.L., A.-K.S., T.E. and P.G.L. contributed to data accessibility and revision of the manuscript.

Corresponding author

Correspondence to Julia W. Y. Kam.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information: Primary Handling Editor: Marike Schiffer.

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Results, Supplementary Fig. 1 and Supplementary Tables 1 and 2.

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kam, J.W.Y., Lin, J.J., Solbakk, AK. et al. Default network and frontoparietal control network theta connectivity supports internal attention. Nat Hum Behav 3, 1263–1270 (2019). https://doi.org/10.1038/s41562-019-0717-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41562-019-0717-0

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing