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Differences in Large-scale and Sliding-window-based Functional Networks of Reappraisal and Suppression

  • Jun, Suhnyoung (Department of Psychology, Yonsei University) ;
  • Lee, Seung-Koo (Department of Radiology, College of Medicine, Yonsei University) ;
  • Han, Sanghoon (Department of Psychology, Yonsei University)
  • Received : 2018.06.18
  • Accepted : 2018.09.19
  • Published : 2018.09.30

Abstract

The process model of emotion regulation suggests that cognitive reappraisal and expressive suppression engage at different time points in the regulation process. Although multiple brain regions and networks have been identified for each strategy, no articles have explored changes in network characteristics or network connectivity over time. The present study examined (a) the whole-brain network and six other resting-state networks, (b) their modularity and global efficiency, which is an index of the efficiency of information exchange across the network, (c) the degree and betweenness centrality for 160 brain regions to identify the hub nodes with the most control over the entire network, and (d) the intra-network and inter-network functional connectivity (FC). Such investigations were performed using a traditional large-scale FC analysis and a relatively recent sliding window correlation analysis. The results showed that the right inferior orbitofrontal cortex was the hub region of the whole-brain network for both strategies. The present findings of temporally altering functional activity of the networks revealed that the default mode network (DMN) activated at the early stage of reappraisal, followed by the task-positive networks (cingulo-opercular network and fronto-parietal network), emotion-processing networks (the cerebellar network and DMN), and sensorimotor network (SMN) that activated at the early stage of suppression, followed by the greater recruitment of task-positive networks and their functional connection with the emotional response-related networks (SMN and occipital network). This is the first study that provides neuroimaging evidence supporting the process model of emotion regulation by revealing the temporally varying network efficiency and intra- and inter-network functional connections of reappraisal and suppression.

Keywords

References

  1. Allen, E. A., Damaraju, E., Plis, S. M., Erhardt, E. B., Eichele, T., & Calhoun, V. D. (2014). Tracking whole-brain connectivity dynamics in the resting state. Cerebral Cortex, 24(3), 663-676. DOI: 10.1093/cercor/bhs352
  2. Anand, B. K., Malhotra, C. L., Singh, B., & Dua, S. (1959). Cerebellar projections to limbic system. Journal of Neurophysiology, 22(4), 451-457. DOI: 10.1152/jn.1959.22.4.451
  3. Andrews-Hanna, J. R. (2012). The brain's default network and its adaptive role in internal mentation. Neuroscientist, 18(3), 251-270. DOI: 10.1177/1073858411403316
  4. Andrews-Hanna, J. R., Smallwood, J., & Spreng, R. N. (2014). The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Annals of the New York Academy of Sciences, 1316, 29-52. DOI: 10.1111/nyas.12360
  5. Bassett, D. S., Wymbs, N. F., Porter, M. A., Mucha, P. J., Carlson, J. M., & Grafton, S. T. (2011). Dynamic reconfiguration of human brain networks during learning. Proceedings of the National Academy of Sciences of the United States of America, 108(18), 7641-7646. DOI: 10.1073/pnas.1018985108
  6. Beck, A. T., & Steer, R. (1988). Beck anxiety inventory (BAI). BiB 2010, 54.
  7. Boissoneault, J., Letzen, J., Lai, S., Robinson, M. E., & Staud, R. (2018). Static and dynamic functional connectivity in patients with chronic fatigue syndrome: use of arterial spin labelling fMRI. Clinical Physiology and Functional Imaging, 38(1), 128-137. DOI: 10.1111/cpf.12393
  8. Braun, U., Schafer, A., Walter, H., Erk, S., Romanczuk-Seiferth, N., Haddad, L., ... Bassett, D. S. (2015). Dynamic reconfiguration of frontal brain networks during executive cognition in humans. Proceedings of the National Academy of Sciences of the United States of America, 112(37), 11678-11683. DOI: 10.1073/pnas.1422487112
  9. Brissenden, J. A., Levin, E. J., Osher, D. E., Halko, M. A., & Somers, D. C. (2016). Functional Evidence for a Cerebellar Node of the Dorsal Attention Network. Journal of Neuroscience, 36(22), 6083-6096. DOI: 10.1523/JNEUROSCI.0344-16.2016
  10. Buckner, R. L., Krienen, F. M., Castellanos, A., Diaz, J. C., & Yeo, B. T. (2011). The organization of the human cerebellum estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106(5), 2322-2345. DOI: 10.1152/jn.00339.2011
  11. Bullmore, E., & Sporns, O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10(3), 186-198. DOI: 10.1038/nrn2575
  12. Butler, A. J., & James, K. H. (2010). The neural correlates of attempting to suppress negative versus neutral memories. Cognitive, Affective, & Behavioral Neuroscience, 10(2), 182-194. DOI: 10.3758/CABN.10.2.182
  13. Chang, C., & Glover, G. H. (2010). Time-frequency dynamics of resting-state brain connectivity measured with fMRI. Neuroimage, 50(1), 81-98. DOI: 10.1016/j.neuroimage.2009.12.011
  14. Cole, M. W., Reynolds, J. R., Power, J. D., Repovs, G., Anticevic, A., & Braver, T. S. (2013). Multi-task connectivity reveals flexible hubs for adaptive task control. Nature Neuroscience, 16(9), 1348-1355. DOI: 10.1038/nn.3470
  15. Cutuli, D. (2014). Cognitive reappraisal and expressive suppression strategies role in the emotion regulation: an overview on their modulatory effects and neural correlates. Frontiers in Systems Neuroscience, 8, 175. DOI: 10.3389/fnsys.2014.00175
  16. Damaraju, E., Allen, E. A., Belger, A., Ford, J. M., McEwen, S., Mathalon, D. H., ... Calhoun, V. D. (2014). Dynamic functional connectivity analysis reveals transient states of dysconnectivity in schizophrenia. NeuroImage: Clinical, 5, 298-308. DOI: 10.1016/j.nicl.2014.07.003
  17. De Vico Fallani, F., Richiardi, J., Chavez, M., & Achard, S. (2014). Graph analysis of functional brain networks: practical issues in translational neuroscience. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1653). DOI: 10.1098/rstb.2013.0521
  18. Dempesy, C. W., Tootle, D. M., Fontana, C. J., Fitzjarrell, A. T., Garey, R. E., & Heath, R. G. (1983). Stimulation of the paleocerebellar cortex of the cat: increased rate of synthesis and release of catecholamines at limbic sites. Biological Psychiatry, 18(1), 127-132.
  19. Di, X., & Biswal, B. B. (2015). Dynamic brain functional connectivity modulated by resting-state networks. Brain Structure and Function, 220(1), 37-46. DOI: 10.1007/s00429-013-0634-3
  20. Di, X., Fu, Z., Chan, S. C., Hung, Y. S., Biswal, B. B., & Zhang, Z. (2015). Task-related functional connectivity dynamics in a block-designed visual experiment. Frontiers in Human Neuroscience, 9, 543. DOI: 10.3389/fnhum.2015.00543
  21. Dosenbach, N. U., Fair, D. A., Miezin, F. M., Cohen, A. L., Wenger, K. K., Dosenbach, R. A., . . . Petersen, S. E. (2007). Distinct brain networks for adaptive and stable task control in humans. Proceedings of the National Academy of Sciences of the United States of America, 104(26), 11073-11078. DOI: 10.1073/pnas.0704320104
  22. Dosenbach, N. U., Nardos, B., Cohen, A. L., Fair, D. A., Power, J. D., Church, J. A., ... Schlaggar, B. L. (2010). Prediction of individual brain maturity using fMRI. Science, 329(5997), 1358-1361. DOI: 10.1126/science.1194144
  23. Dosenbach, N. U., Visscher, K. M., Palmer, E. D., Miezin, F. M., Wenger, K. K., Kang, H. C., . . . Petersen, S. E. (2006). A core system for the implementation of task sets. Neuron, 50(5), 799-812. DOI: 10.1016/j.neuron.2006.04.031
  24. Dum, R. P., & Strick, P. L. (2003). An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. Journal of Neurophysiology, 89(1), 634-639. DOI: 10.1152/jn.00626.2002
  25. Fair, D. A., Cohen, A. L., Power, J. D., Dosenbach, N. U., Church, J. A., Miezin, F. M., . . . Petersen, S. E. (2009). Functional brain networks develop from a "local to distributed" organization. PLoS Computational Biology, 5(5), e1000381. DOI: 10.1371/journal.pcbi.1000381
  26. Fornito, A., Harrison, B. J., Zalesky, A., & Simons, J. S. (2012). Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection. Proceedings of the National Academy of Sciences of the United States of America, 109(31), 12788-12793. DOI: 10.1073/pnas.1204185109
  27. Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S., & Turner, R. (1996). Movement-related effects in fMRI time-series. Magnetic Resonance in Medicine, 35(3), 346-355. https://doi.org/10.1002/mrm.1910350312
  28. Gagnepain, P., Hulbert, J., & Anderson, M. C. (2017). Parallel Regulation of Memory and Emotion Supports the Suppression of Intrusive Memories. Journal of Neuroscience, 37(27), 6423-6441. DOI: 10.1523/JNEUROSCI.2732-16.2017
  29. Glickstein, M. (2007). What does the cerebellum really do? Current Biology, 17(19), R824-827. DOI: 10.1016/j.cub.2007.08.009
  30. Gross, J. J. (2002). Emotion regulation: affective, cognitive, and social consequences. Psychophysiology, 39(3), 281-291. DOI: 10.1017.S0048577201393198 https://doi.org/10.1017/S0048577201393198
  31. Gross, J. J., & John, O. P. (1998). Mapping the domain of expressivity: multimethod evidence for a hierarchical model. Journal of Personality and Social Psychology, 74(1), 170-191. https://doi.org/10.1037/0022-3514.74.1.170
  32. Gross, J. J., & John, O. P. (2003). Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. Journal of Personality and Social Psychology, 85(2), 348-362. https://doi.org/10.1037/0022-3514.85.2.348
  33. Hayes, J. P., Morey, R. A., Petty, C. M., Seth, S., Smoski, M. J., McCarthy, G., & Labar, K. S. (2010). Staying cool when things get hot: emotion regulation modulates neural mechanisms of memory encoding. Frontiers in Human Neuroscience, 4, 230. DOI: 10.3389/fnhum.2010.00230
  34. Hofmann, S. G., Heering, S., Sawyer, A. T., & Asnaani, A. (2009). How to handle anxiety: The effects of reappraisal, acceptance, and suppression strategies on anxious arousal. Behaviour Research and Therapy, 47(5), 389-394. DOI: 10.1016/j.brat.2009.02.010
  35. Hutchison, R. M., Womelsdorf, T., Allen, E. A., Bandettini, P. A., Calhoun, V. D., Corbetta, M., ... Chang, C. (2013). Dynamic functional connectivity: promise, issues, and interpretations. Neuroimage, 80, 360-378. DOI: 10.1016/j.neuroimage.2013.05.079
  36. Hutchison, R. M., Womelsdorf, T., Gati, J. S., Everling, S., & Menon, R. S. (2013). Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Human Brain Mapping, 34(9), 2154-2177. DOI: 10.1002/hbm.22058
  37. Jones, D. T., Vemuri, P., Murphy, M. C., Gunter, J. L., Senjem, M. L., Machulda, M. M., ... Jack, C. R., Jr. (2012). Non-stationarity in the "resting brain's" modular architecture. PLoS One, 7(6), e39731. DOI: 10.1371/journal.pone.0039731
  38. Kelly, R. M., & Strick, P. L. (2003). Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. Journal of Neuroscience, 23(23), 8432-8444. https://doi.org/10.1523/JNEUROSCI.23-23-08432.2003
  39. Kiviniemi, V., Vire, T., Remes, J., Elseoud, A. A., Starck, T., Tervonen, O., & Nikkinen, J. (2011). A sliding time-window ICA reveals spatial variability of the default mode network in time. Brain Connectivity, 1(4), 339-347. DOI: 10.1089/brain.2011.0036
  40. Lazarus, R. S., & Alfert, E. (1964). Short-Circuiting of Threat by Experimentally Altering Cognitive Appraisal. Journal of Abnormal Psychology, 69, 195-205. https://doi.org/10.1037/h0044635
  41. Marcinkiewicz, M., Morcos, R., & Chretien, M. (1989). CNS connections with the median raphe nucleus: retrograde tracing with WGA-apoHRP-Gold complex in the rat. Journal of Comparative Neurology, 289(1), 11-35. DOI: 10.1002/cne.902890103
  42. Middleton, F. A., & Strick, P. L. (2001). Cerebellar projections to the prefrontal cortex of the primate. Journal of Neuroscience, 21(2), 700-712. https://doi.org/10.1523/JNEUROSCI.21-02-00700.2001
  43. Ochsner, K. N., & Gross, J. J. (2008). Cognitive Emotion Regulation: Insights from Social Cognitive and Affective Neuroscience. Current Directions in Psychological Science, 17(2), 153-158. DOI: 10.1111/j.1467-8721.2008.00566.x
  44. Ochsner, K. N., Ray, R. D., Cooper, J. C., Robertson, E. R., Chopra, S., Gabrieli, J. D., & Gross, J. J. (2004). For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. Neuroimage, 23(2), 483-499. DOI: 10.1016/j.neuroimage.2004.06.030
  45. Pan, J., Zhan, L., Hu, C., Yang, J., Wang, C., Gu, L., ... Wu, X. (2018). Emotion Regulation and Complex Brain Networks: Association Between Expressive Suppression and Efficiency in the Fronto-Parietal Network and Default-Mode Network. Frontiers in Human Neuroscience, 12, 70. DOI: 10.3389/fnhum.2018.00070
  46. Petrican, R., Rosenbaum, R. S., & Grady, C. (2015). Expressive suppression and neural responsiveness to nonverbal affective cues. Neuropsychologia, 77, 321-330. DOI: 10.1016/j.neuropsychologia.2015.09.013
  47. Ramos-Nunez, A. I., Fischer-Baum, S., Martin, R. C., Yue, Q., Ye, F., & Deem, M. W. (2017). Static and Dynamic Measures of Human Brain Connectivity Predict Complementary Aspects of Human Cognitive Performance. Frontiers in Human Neuroscience, 11, 420. DOI: 10.3389/fnhum.2017.00420
  48. Rogers, B. P., Morgan, V. L., Newton, A. T., & Gore, J. C. (2007). Assessing functional connectivity in the human brain by fMRI. Magnetic Resonance Imaging, 25(10), 1347-1357. DOI: 10.1016/j.mri.2007.03.007
  49. Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: uses and interpretations. Neuroimage, 52(3), 1059-1069. DOI: 10.1016/j.neuroimage.2009.10.003
  50. Sadaghiani, S., Scheeringa, R., Lehongre, K., Morillon, B., Giraud, A. L., D'Esposito, M., & Kleinschmidt, A. (2012). alpha-band phase synchrony is related to activity in the fronto-parietal adaptive control network. Journal of Neuroscience, 32(41), 14305-14310. DOI: 10.1523/JNEUROSCI.1358-12.2012
  51. Sakoglu, U., Pearlson, G. D., Kiehl, K. A., Wang, Y. M., Michael, A. M., & Calhoun, V. D. (2010). A method for evaluating dynamic functional network connectivity and task-modulation: application to schizophrenia. MAGMA, 23(5-6), 351-366. DOI: 10.1007/s10334-010-0197-8
  52. Schmahmann, J. D., & Caplan, D. (2006). Cognition, emotion and the cerebellum. Brain, 129(Pt 2), 290-292. DOI: 10.1093/brain/awh729
  53. Schutter, D. J., & van Honk, J. (2005). The cerebellum on the rise in human emotion. Cerebellum, 4(4), 290-294. DOI: 10.1080/14734220500348584
  54. Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., ... Greicius, M. D. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience, 27(9), 2349-2356. DOI: 10.1523/JNEUROSCI.5587-06.2007
  55. Sheppes, G., & Gross, J. J. (2011). Is timing everything? Temporal considerations in emotion regulation. Personality and Social Psychology Review, 15(4), 319-331. DOI: 10.1177/1088868310395778
  56. Shirer, W. R., Ryali, S., Rykhlevskaia, E., Menon, V., & Greicius, M. D. (2012). Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cerebral Cortex, 22(1), 158-165. DOI: 10.1093/cercor/bhr099
  57. Stoffers, D., Diaz, B. A., Chen, G., den Braber, A., van't Ent, D., Boomsma, D. I., ... Linkenkaer-Hansen, K. (2015). Resting-State fMRI Functional Connectivity Is Associated with Sleepiness, Imagery, and Discontinuity of Mind. PLoS One, 10(11), e0142014. DOI: 10.1371/journal.pone.0142014
  58. Takeuchi, H., Taki, Y., Nouchi, R., Yokoyama, R., Kotozaki, Y., Nakagawa, S., ... Kawashima, R. (2017). Regional homogeneity, resting-state functional connectivity and amplitude of low frequency fluctuation associated with creativity measured by divergent thinking in a sex-specific manner. Neuroimage, 152, 258-269. DOI: 10.1016/j.neuroimage.2017.02.079
  59. Turner, B. M., Paradiso, S., Marvel, C. L., Pierson, R., Boles Ponto, L. L., Hichwa, R. D., & Robinson, R. G. (2007). The cerebellum and emotional experience. Neuropsychologia, 45(6), 1331-1341. DOI: 10.1016/j.neuropsychologia.2006.09.023
  60. van den Heuvel, M. P., & Hulshoff Pol, H. E. (2010). Exploring the brain network: a review on restingstate fMRI functional connectivity. European Neuropsychopharmacology, 20(8), 519-534. DOI: 10.1016/j.euroneuro.2010.03.008
  61. Wang, Y., Yang, L., & Wang, Y. (2014). Suppression (but not reappraisal) impairs subsequent error detection: an ERP study of emotion regulation's resource-depleting effect. PLoS One, 9(4), e96339. DOI: 10.1371/journal.pone.0096339
  62. Yan, C. G., Cheung, B., Kelly, C., Colcombe, S., Craddock, R. C., Di Martino, A., ... Milham, M. P. (2013). A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage, 76, 183-201. DOI: 10.1016/j.neuroimage.2013.03.004
  63. Zaki, J., Hennigan, K., Weber, J., & Ochsner, K. N. (2010). Social cognitive conflict resolution: contributions of domain-general and domainspecific neural systems. Journal of Neuroscience, 30(25), 8481-8488. DOI: 10.1523/JNEUROSCI.0382-10.2010