Abstract
The frontoparietal control network (FPCN) plays a central role in tuning connectivity between brain networks to achieve integrated cognitive processes. It has been proposed that two subnetworks within the FPCN separately regulate two antagonistic networks: the FPCNa is connected to the default network (DN) that deals with internally oriented introspective processes, whereas the FPCNb is connected to the dorsal attention network (DAN) that deals with externally oriented perceptual attention. However, cooperation between the DN and DAN induced by distinct task demands has not been well-studied. Here, we characterized the dynamic cooperation among the DN, DAN, and two FPCN subnetworks in a task in which internally oriented self-referential processing could facilitate externally oriented visual working memory. Functional connectivity analysis showed enhanced coupling of a circuit from the DN to the FPCNa, then to the FPCNb, and finally to the DAN when the self-referential processing improved memory recognition in high self-referential conditions. The direct connection between the DN and DAN was not enhanced. This circuit could be reflected by an increased chain-mediating effect of the FPCNa and the FPCNb between the DN and DAN in high self-referential conditions. Graph analysis revealed that high self-referential conditions were accompanied by increased global and local efficiencies, and the increases were mainly driven by the increased efficiency of FPCN nodes. Together, our findings extend prior observations and indicate that the coupling between the two FPCN subnetworks serves as a bridge between the DN and DAN, supporting the interaction between internally oriented and externally oriented processes.
Similar content being viewed by others
Data availability
The data and code in the study are available from the corresponding author upon direct request, with a formal data-sharing agreement.
Code availability
Scripts used for running experiments and data analyses are available upon request to the corresponding author.
References
Andrews-Hanna JR, Smallwood J, Spreng RN (2014) The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Ann NY Acad Sci 1316:29–52. https://doi.org/10.1111/nyas.12360
Anticevic A, Cole MW, Murray JD, Corlett PR, Wang X-J, Krystal JH (2012) The role of default network deactivation in cognition and disease. Trends Cogn Sci 16:584–592. https://doi.org/10.1016/j.tics.2012.10.008
Barrouillet P, Bernardin S, Camos V (2004) Time constraints and resource sharing in adults’ working memory spans. J Exp Psychol Gen 133:83–100. https://doi.org/10.1037/0096-3445.133.1.83
Bassett DS, Sporns O (2017) Network neuroscience. Nat Neurosci 20:353–364. https://doi.org/10.1038/nn.4502
Bertolero MA, Yeo BTT, D’Esposito M (2015) The modular and integrative functional architecture of the human brain. Proc Natl Acad Sci USA 112:E6798–E6807. https://doi.org/10.1073/pnas.1510619112
Bertolero MA, Yeo BTT, Bassett DS, D’Esposito M (2018) A mechanistic model of connector hubs, modularity and cognition. Nat Hum Behav 2:765–777. https://doi.org/10.1038/s41562-018-0420-6
Braun U, Schäfer A, Walter H, Erk S, Romanczuk-Seiferth N, Haddad L, Schweiger JI, Grimm O, Heinz A, Tost H, Meyer-Lindenberg A, Bassett DS (2015) Dynamic reconfiguration of frontal brain networks during executive cognition in humans. Proc Natl Acad Sci USA 112:11678–11683. https://doi.org/10.1073/pnas.1422487112
Buckner RL, DiNicola LM (2019) The brain’s default network: updated anatomy, physiology and evolving insights. Nat Rev Neurosci 20:593–608. https://doi.org/10.1038/s41583-019-0212-7
Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198. https://doi.org/10.1038/nrn2618
Buuren MV, Gladwin TE, Zandbelt BB, Kahn RS, Vink M (2010) Reduced functional coupling in the default-mode network during self-referential processing. Hum Brain Mapp 31:1117–1127. https://doi.org/10.1002/hbm.20920
Chen AC, Oathes DJ, Chang C, Bradley T, Zhou Z-W, Williams LM, Glover GH, Deisseroth K, Etkin A (2013) Causal interactions between fronto-parietal central executive and default-mode networks in humans. Proc Natl Acad Sci USA 110:19944–19949. https://doi.org/10.1073/pnas.1311772110
Cocchi L, Zalesky A, Fornito A, Mattingley JB (2013) Dynamic cooperation and competition between brain systems during cognitive control. Trends Cogn Sci 17:493–501. https://doi.org/10.1016/j.tics.2013.08.006
Cocuzza CV, Ito T, Schultz D, Bassett DS, Cole MW (2020) Flexible coordinator and switcher hubs for adaptive task control. J Neurosci 40:6949–6968. https://doi.org/10.1523/JNEUROSCI.2559-19.2020
Cole MW, Schneider W (2007) The cognitive control network: Integrated cortical regions with dissociable functions. Neuroimage 37:343–360. https://doi.org/10.1016/j.neuroimage.2007.03.071
Cole MW, Bassett DS, Power JD, Braver TS, Petersen SE, Cole MW (2014) Intrinsic and task-evoked network architectures of the human brain. Neuron 83:238–251. https://doi.org/10.1016/j.neuron.2014.05.014
Cole MW, Reynolds JR, Power JD, Repovs G, Anticevic A, Braver TS (2013) Multi-task connectivity reveals flexible hubs for adaptive task control. Nat Neurosci 16:1348–1355. https://doi.org/10.1038/nn.3470
Corbetta M, Patel G, Shulman GL (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58:306–324. https://doi.org/10.1016/j.neuron.2008.04.017
D’Esposito M, Postle BR (2015) The cognitive neuroscience of working memory. Annu Rev Psychol 66:115–142. https://doi.org/10.1146/annurev-psych-010814-015031
Damoiseaux JS, Rombouts SARB, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848–13853. https://doi.org/10.1073/pnas.0601417103
Davey CG, Pujol J, Harrison BJ (2016) Mapping the self in the brain’s default mode network. Neuroimage 132:390–397. https://doi.org/10.1016/j.neuroimage.2016.02.022
Dixon ML, Andrews-Hanna JR, Spreng RN, Irving ZC, Mills C, Girn M, Christoff K (2017) Interactions between the default network and dorsal attention network vary across default subsystems, time, and cognitive states. Neuroimage 147:632–649. https://doi.org/10.1016/j.neuroimage.2016.12.073
Dixon ML, De La Vega A, Mills C, Andrews-Hanna J, Spreng RN, Cole MW, Christoff K (2018) Heterogeneity within the frontoparietal control network and its relationship to the default and dorsal attention networks. Proc Natl Acad Sci USA 115:E1598–E1607. https://doi.org/10.1073/pnas.1715766115
Dosenbach NUF, Fair DA, Cohen AL, Schlaggar BL, Petersen SE (2008) A dual-networks architecture of top-down control. Trends Cogn Sci 12:99–105. https://doi.org/10.1016/j.tics.2008.01.001
Ellamil M, Fox KCR, Dixon ML, Pritchard S, Todd RM, Thompson E, Christoff K (2016) Dynamics of neural recruitment surrounding the spontaneous arising of thoughts in experienced mindfulness practitioners. Neuroimage 136:186–196. https://doi.org/10.1016/j.neuroimage.2016.04.034
Fornito A, Harrison BJ, Zalesky A, Simons JS (2012) Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection. Proc Natl Acad Sci USA 109:12788–12793. https://doi.org/10.1073/pnas.1204185109
Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711. https://doi.org/10.1038/nrn2201
Fox KCR, Spreng RN, Ellamil M, Andrews-Hanna JR, Christoff K (2015) The wandering brain: Meta-analysis of functional neuroimaging studies of mind-wandering and related spontaneous thought processes. Neuroimage 111:611–621. https://doi.org/10.1016/j.neuroimage.2015.02.039
Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673–9678. https://doi.org/10.1073/pnas.0504136102
Fransson P (2005) Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis. Hum Brain Mapp 26:15–29. https://doi.org/10.1002/hbm.20113
Gazzaley A, Nobre AC (2012) Top-down modulation: bridging selective attention and working memory. Trends Cogn Sci 16:129–135. https://doi.org/10.1016/j.tics.2011.11.014
Gerlach KD, Spreng RN, Gilmore AW, Schacter DL (2011) Solving future problems: default network and executive activity associated with goal-directed mental simulations. Neuroimage 55:1816–1824. https://doi.org/10.1016/j.neuroimage.2011.01.030
Golland Y, Bentin S, Gelbard H, Benjamini Y, Heller R, Nir Y, Hasson U, Malach R (2007) Extrinsic and intrinsic systems in the posterior cortex of the human brain revealed during natural sensory stimulation. Cereb Cortex 17:766–777. https://doi.org/10.1093/cercor/bhk030
Gu S, Pasqualetti F, Cieslak M, Telesford QK, Yu AB, Kahn AE, Medaglia JD, Vettel JM, Miller MB, Grafton ST, Bassett DS (2015) Controllability of structural brain networks. Nat Commun 6:8414. https://doi.org/10.1038/ncomms9414
Hayes AF (2013) Introduction to mediation, moderation, and conditional process analysis: a regression-based approach. Guilford publications, New York
Kam JWY, Lin JJ, Solbakk A-K, Endestad T, Larsson PG, Knight RT (2019) Default network and frontoparietal control network theta connectivity supports internal attention. Nat Hum Behav 3:1263–1270. https://doi.org/10.1038/s41562-019-0717-0
Keerativittayayut R, Aoki R, Sarabi MT, Jimura K, Nakahara K (2018) Large-scale network integration in the human brain tracks temporal fluctuations in memory encoding performance. Elife 7:e32696. https://doi.org/10.7554/eLife.32696
Kiyonaga A, Egner T (2013) Working memory as internal attention: toward an integrative account of internal and external selection processes. Psychon Bull Rev 20:228–242. https://doi.org/10.3758/s13423-012-0359-y
Mencarelli L, Neri F, Momi D, Menardi A, Rossi S, Rossi A, Santarnecchi E (2019) Stimuli, presentation modality, and load-specific brain activity patterns during n-back task. Hum Brain Mapp 40:3810–3831. https://doi.org/10.1002/hbm.24633
Miller EK, Buschman TJ (2013) Cortical circuits for the control of attention. Curr Opin Neurobiol 23:216–222. https://doi.org/10.1016/j.conb.2012.11.011
Murphy AC, Bertolero MA, Papadopoulos L, Lydon-Staley DM, Bassett DS (2020) Multimodal network dynamics underpinning working memory. Nat Commun 11(1):3035. https://doi.org/10.1038/s41467-020-15541-0
Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE (2014) Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 84:320–341. https://doi.org/10.1016/j.neuroimage.2013.08.048
Power JD, Cohen AL, Nelson SM, Wig GS, Barnes KA, Church JA, Vogel AC, Laumann TO, Miezin FM, Schlaggar BL, Petersen SE (2011) Functional network organization of the human brain. Neuron 72:665–678. https://doi.org/10.1016/j.neuron.2011.09.006
Ptak R, Schnider A, Fellrath J (2017) The dorsal frontoparietal network: a core system for emulated action. Trends Cogn Sci 21:589–599. https://doi.org/10.1016/j.tics.2017.05.002
Raichle ME (2015) The brain’s default mode network. Annu Rev Neurosci 38:433–447. https://doi.org/10.1146/annurev-neuro-071013-014030
Shine James M, Bissett Patrick G, Bell Peter T, Koyejo O, Balsters Joshua H, Gorgolewski Krzysztof J, Moodie Craig A, Poldrack Russell A (2016) The dynamics of functional brain networks: Integrated network states during cognitive task performance. Neuron 92:544–554. https://doi.org/10.1016/j.neuron.2016.09.018
Smallwood J, Brown K, Baird B, Schooler JW (2012) Cooperation between the default mode network and the frontal–parietal network in the production of an internal train of thought. Brain Res 1428:60–70. https://doi.org/10.1016/j.brainres.2011.03.072
Sporns O (2014) Contributions and challenges for network models in cognitive neuroscience. Nat Neurosci 17:652–660. https://doi.org/10.1038/nn.3690
Spreng RN, DuPre E, Selarka D, Garcia J, Gojkovic S, Mildner J, Luh W-M, Turner GR (2014) Goal-congruent default network activity facilitates cognitive control. J Neurosci 34:14108–14114. https://doi.org/10.1523/JNEUROSCI.2815-14.2014
Spreng RN, Stevens WD, Chamberlain JP, Gilmore AW, Schacter DL (2010) Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition. Neuroimage 53:303–317. https://doi.org/10.1016/j.neuroimage.2010.06.016
Sui J, He X, Humphreys GW (2012) Perceptual effects of social salience: evidence from self-prioritization effects on perceptual matching. J Exp Psychol Hum Percept Perform 38:1105–1117. https://doi.org/10.1037/a0029792
Szczepanski SM, Pinsk MA, Douglas MM, Kastner S, Saalmann YB (2013) Functional and structural architecture of the human dorsal frontoparietal attention network. Proc Natl Acad Sci USA 110:15806–15811. https://doi.org/10.1073/pnas.1313903110
Wang J, Wang X, Xia M, Liao X, Evans A, He Y (2015) GRETNA: a graph theoretical network analysis toolbox for imaging connectomics. Front Hum Neurosci 9:386. https://doi.org/10.3389/fnhum.2015.00386
Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL, Smoller JW, Zöllei L, Polimeni JR (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 106:1125–1165. https://doi.org/10.1152/jn.00338.2011
Yin S, Bi T, Chen A, Egner T (2021) Ventromedial prefrontal cortex drives the prioritization of self-associated stimuli in working memory. J Neurosci 41:2012–2023. https://doi.org/10.1523/JNEUROSCI.1783-20.2020
Yin S, Sui J, Chiu Y-C, Chen A, Egner T (2019) Automatic prioritization of self-referential stimuli in working memory. Psychol Sci 30:415–423. https://doi.org/10.1177/0956797618818483
Acknowledgements
The authors are grateful to Matthew L. Dixon for providing the brain template files of regions of interest used in the present analyses. This work was supported by grants from the National Natural Science Foundation of China (32171040, 32000783), and Natural Science Foundation of Chongqing, China (cstc2020jcyj-bshX0120), and the fellowship of China National Postdoctoral Program for Innovative Talents (BX20200283).
Funding
This work was supported by grants from the National Natural Science Foundation of China (32171040, 32000783), and Natural Science Foundation of Chongqing, China (cstc2020jcyj-bshX0120), and the fellowship of China National Postdoctoral Program for Innovative Talents (BX20200283).
Author information
Authors and Affiliations
Contributions
SY and AC initially conceived and designed the experiments. SY and YL performed the experiments. The data were analyzed by SY and YL, and the paper was written by SY, YL, and AC.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
The study was approved by the University Human Ethics Committee of Southwest University (China).
Consent to participate
All volunteers gave the informed written consent and were compensated for their participation.
Consent for publication
The participant has consented to the submission of the case report to the journal.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Yin, S., Li, Y. & Chen, A. Functional coupling between frontoparietal control subnetworks bridges the default and dorsal attention networks. Brain Struct Funct 227, 2243–2260 (2022). https://doi.org/10.1007/s00429-022-02517-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-022-02517-7