Abstract
Self-regulation, which is an individual’s ability to control their emotions and behaviors in pursuit of goals, is a complex cognitive function that relies on distributed brain networks. Here, we used activation likelihood estimation (ALE) to conduct two large-scale meta-analyses of brain imaging studies of emotional regulation and behavioral regulation. We used single analysis of ALE to identify brain activation regions associated with behavioral regulation and emotion regulation. The conjunction results of the contrast analysis of the two domains showed that the crucial brain regions of dorsal anterior cingulate cortex (dACC), bilateral anterior insula (AI), and right inferior parietal lobule (IPL) are nested within the brain areas of the two regulation domains at the spatial and functional level. In addition, we assessed the coactivation pattern of the four common regions using meta-analytic connectivity modeling (MACM). The coactivation brain patterns based on the dACC and bilateral AI overlapped with the two regulation brain maps in a high proportion. Furthermore, the functional characters of the identified common regions were reverse-inferenced using the BrainMap database. Collectively, these results indicate that the brain regions of dACC and bilateral AI, playing a crucial role as a hub to other brain regions and networks by effective connectivity in self-regulation, are spatially nested in the brain network of behavioral regulation and emotion regulation.





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References
Abbing A, de Sonneville L, Baars E, Bourne D, Swaab H (2019) Anxiety reduction through art therapy in women Exploring stress regulation and executive functioning as underlying neurocognitive mechanisms. PloS One 14(12):e0225200. https://doi.org/10.1371/journal.pone.0225200
Barrett LF, Simmons WK (2015) Interoceptive predictions in the brain. Nat Rev Neurosci 16(7):419–429. https://doi.org/10.1038/nrn3950
Bellucci G, Feng C, Camilleri J, Eickhoff SB, Krueger F (2018) The role of the anterior insula in social norm compliance and enforcement: evidence from coordinate-based and functional connectivity meta-analyses. Neurosci Biobehav Rev 92:378–389. https://doi.org/10.1016/j.neubiorev.2018.06.024
Boccadoro S, Wagels L, Puiu AA, Votinov M, Weidler C, Veselinovic T, Demko Z, Raine A, Neuner I (2021) A meta-analysis on shared and distinct neural correlates of the decision-making underlying altruistic and retaliatory punishment. Hum Brain Mapp 42(17):5547–5562. https://doi.org/10.1002/hbm.25635
Caspers S, Zilles K, Laird AR, Eickhoff SB (2010) ALE meta-analysis of action observation and imitation in the human brain. Neuroimage 50(3):1148–1167. https://doi.org/10.1016/j.neuroimage.2009.12.112
Cohen JR, Berkman ET, Lieberman MD (2013) Intentional and incidental self-control in ventrolateral PFC. In: Stuss DT, Knight RT (eds) Principles of frontal lobe function. Oxford University Press, New York, USA, pp 417–440
Contreras-Osorio F, Ramirez-Campillo R, Cerda-Vega E, Campos-Jara R, Martínez-Salazar C, Reigal RE, Hernández-Mendo A, Carneiro L, Campos-Jara C (2022) Effects of physical exercise on executive function in adults with depression: a systematic review and meta-analysis. Int J Environ Res Public Health 19(22):15270. https://doi.org/10.3390/ijerph192215270
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215. https://doi.org/10.1038/nrn755
Craig AD (2009) How do you feel–now? The anterior insula and human awareness. Nat Rev Neurosci 10(1):59–70. https://doi.org/10.1038/nrn2555
Critchley HD, Harrison NA (2013) Visceral influences on brain and behavior. Neuron 77(4):624–638. https://doi.org/10.1016/j.neuron.2013.02.008
Desmurget M, Sirigu A (2009) A parietal-premotor network for movement intention and motor awareness. Trends Cogn Sci 13(10):411–419. https://doi.org/10.1016/j.tics.2009.08.001
Desmurget M, Sirigu A (2012) Conscious motor intention emerges in the inferior parietal lobule. Curr Opin Neurobiol 22(6):1004–1011. https://doi.org/10.1016/j.conb.2012.06.006
Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT (2012) Activation likelihood estimation meta-analysis revisited. Neuroimage 59(3):2349–2361. https://doi.org/10.1016/j.neuroimage.2011.09.017
Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30(9):2907–2926. https://doi.org/10.1002/hbm.20718
Eklund A, Nichols TE, Knutsson H (2016) Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci USA 113(28):7900–7905. https://doi.org/10.1073/pnas.1602413113
Evans AC, Kamber M, Collins DL, MacDonald D (1994) An MRI-based probabilistic atlas of neuroanatomy. Magnetic resonance scanning and epilepsy. Springer, Boston, MA, pp 263–274. https://doi.org/10.1007/978-1-4615-2546-2_48
Frewen P, Schroeter ML, Riva G, Cipresso P, Fairfield B, Padulo C, Kemp AH, Palaniyappan L, Owolabi M, Kusi-Mensah K, Polyakova M, Fehertoi N, D’Andrea W, Lowe L, Northoff G (2020) Neuroimaging the consciousness of self: Review, and conceptual-methodological framework. Neurosci Biobehav Rev 112:164–212. https://doi.org/10.1016/j.neubiorev.2020.01.023
Gross JJ (1998) The emerging field of emotion regulation: an integrative review. Rev General Psychol 2(3):271–299. https://doi.org/10.1037/1089-2680.2.3.271
Heatherton TF, Wagner DD (2011) Cognitive neuroscience of self-regulation failure. Trends Cogn Sci 15(3):132–139. https://doi.org/10.1016/j.tics.2010.12.005
Heilbronner SR, Hayden BY (2016) Dorsal anterior cingulate cortex: a bottom-up view. Annu Rev Neurosci 39:149–170. https://doi.org/10.1146/annurev-neuro-070815-013952
Inzlicht M, Werner KM, Briskin JL, Roberts BW (2021) Integrating models of self-regulation. Annu Rev Psychol 72:319–345. https://doi.org/10.1146/annurev-psych-061020-105721
Johnstone T, van Reekum CM, Urry HL, Kalin NH, Davidson RJ (2007) Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J Neurosci Off J Soc Neurosci 27(33):8877–8884. https://doi.org/10.1523/JNEUROSCI.2063-07.2007
Kim MJ, Whalen PJ (2009) The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. J Neurosci Off J Soc Neurosci 29(37):11614–11618. https://doi.org/10.1523/JNEUROSCI.2335-09.2009
Laird AR, Eickhoff SB, Fox PM, Uecker AM, Ray KL, Saenz JJ Jr, McKay DR, Bzdok D, Laird RW, Robinson JL, Turner JA, Turkeltaub PE, Lancaster JL, Fox PT (2011) The BrainMap strategy for standardization, sharing, and meta-analysis of neuroimaging data. BMC Res Notes 4:349. https://doi.org/10.1186/1756-0500-4-349
Laird AR, Eickhoff SB, Kurth F, Fox PM, Uecker AM, Turner JA, Robinson JL, Lancaster JL, Fox PT (2009) ALE meta-analysis workflows via the brainmap database: progress towards a probabilistic functional brain atlas. Front Neuroinform 3:23. https://doi.org/10.3389/neuro.11.023.2009
Langner R, Leiberg S, Hoffstaedter F, Eickhoff SB (2018) Towards a human self-regulation system: Common and distinct neural signatures of emotional and behavioural control. Neurosci Biobehav Rev 90:400–410. https://doi.org/10.1016/j.neubiorev.2018.04.022
Langner R, Rottschy C, Laird AR, Fox PT, Eickhoff SB (2014) Meta-analytic connectivity modeling revisited: controlling for activation base rates. Neuroimage 99:559–570. https://doi.org/10.1016/j.neuroimage.2014.06.007
Lee TW, Xue SW (2018) Does emotion regulation engage the same neural circuit as working memory? A meta-analytical comparison between cognitive reappraisal of negative emotion and 2-back working memory task. PloS One 13(9):e0203753. https://doi.org/10.1371/journal.pone.0203753
Matsumoto K, Tanaka K (2004) Neuroscience. Conflict and cognitive control. Science (New York, N.Y.) 303(5660):969–970. https://doi.org/10.1126/science.1094733
Menon V (2011) Large-scale brain networks and psychopathology: a unifying triple network model. Trends Cogn Sci 15(10):483–506. https://doi.org/10.1016/j.tics.2011.08.003
Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214(5–6):655–667. https://doi.org/10.1007/s00429-010-0262-0
Miola A, Cattarinussi G, Antiga G, Caiolo S, Solmi M, Sambataro F (2022) Difficulties in emotion regulation in bipolar disorder: a systematic review and meta-analysis. J Affect Disord 302:352–360. https://doi.org/10.1016/j.jad.2022.01.102
Molnar-Szakacs I, Uddin LQ (2022) Anterior insula as a gatekeeper of executive control. Neurosci Biobehav Rev 139:104736. https://doi.org/10.1016/j.neubiorev.2022.104736
Morein-Zamir S, Papmeyer M, Pertusa A, Chamberlain SR, Fineberg NA, Sahakian BJ, Mataix-Cols D, Robbins TW (2014) The profile of executive function in OCD hoarders and hoarding disorder. Psychiatry Res 215(3):659–667. https://doi.org/10.1016/j.psychres.2013.12.026
Morawetz C, Bode S, Derntl B, Heekeren HR (2017) The effect of strategies, goals and stimulus material on the neural mechanisms of emotion regulation: a meta-analysis of fMRI studies. Neurosci Biobehav Rev 72:111–128. https://doi.org/10.1016/j.neubiorev.2016.11.014
Numssen O, Bzdok D, Hartwigsen G (2021) Functional specialization within the inferior parietal lobes across cognitive domains. eLife 10:e63591. https://doi.org/10.7554/eLife.63591
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Moher D (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ (Clinical Res ed) 372:n71. https://doi.org/10.1136/bmj.n71
Paulus MP, Frank LR (2006) Anterior cingulate activity modulates nonlinear decision weight function of uncertain prospects. Neuroimage 30(2):668–677. https://doi.org/10.1016/j.neuroimage.2005.09.061
Picó-Pérez M, Alemany-Navarro M, Dunsmoor JE, Radua J, Albajes-Eizagirre A, Vervliet B, Cardoner N, Benet O, Harrison BJ, Soriano-Mas C, Fullana MA (2019) Common and distinct neural correlates of fear extinction and cognitive reappraisal: A meta-analysis of fMRI studies. Neurosci Biobehav Rev 104:102–115. https://doi.org/10.1016/j.neubiorev.2019.06.029
Popov T, Westner BU, Silton RL, Sass SM, Spielberg JM, Rockstroh B, Heller W, Miller GA (2018) Time course of brain network reconfiguration supporting inhibitory control. J Neurosci Off J Soc Neurosci 38(18):4348–4356. https://doi.org/10.1523/JNEUROSCI.2639-17.2018
Posner MI, Rothbart MK (1998) Attention, self-regulation and consciousness. Phil Trans R Soc Lond Ser B Biol Sci 353(1377):1915–1927. https://doi.org/10.1098/rstb.1998.0344
See CCH, Tan JM, Tan VSY, Sündermann O (2022) A systematic review on the links between emotion regulation difficulties and obsessive-compulsive disorder. J Psychiatr Res 154:341–353. https://doi.org/10.1016/j.jpsychires.2022.07.023
Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci Off J Soc Neurosci 27(9):2349–2356. https://doi.org/10.1523/JNEUROSCI.5587-06.2007
Seth AK (2013) Interoceptive inference, emotion, and the embodied self. Trends Cogn Sci 17(11):565–573. https://doi.org/10.1016/j.tics.2013.09.007
Seth AK, Critchley HD (2013) Extending predictive processing to the body: emotion as interoceptive inference. Behav Brain Sci 36(3):227–228. https://doi.org/10.1017/S0140525X12002270
Shenhav A, Botvinick MM, Cohen JD (2013) The expected value of control: an integrative theory of anterior cingulate cortex function. Neuron 79(2):217–240. https://doi.org/10.1016/j.neuron.2013.07.007
Silton RL, Heller W, Engels AS, Towers DN, Spielberg JM, Edgar JC, Sass SM, Stewart JL, Sutton BP, Banich MT, Miller GA (2011) Depression and anxious apprehension distinguish frontocingulate cortical activity during top-down attentional control. J Abnorm Psychol 120(2):272–285. https://doi.org/10.1037/a0023204
Tournikioti K, Alevizaki M, Michopoulos I, Mantzou A, Soldatos C, Douzenis A, Dikeos D, Ferentinos P (2021) Cortisol to dehydroepiandrosterone sulphate ratio and executive function in bipolar disorder. Neuropsychobiology 80(4):342–351. https://doi.org/10.1159/000513512
Turkeltaub PE, Eden GF, Jones KM, Zeffiro TA (2002) Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage 16(3 Pt 1):765–780. https://doi.org/10.1006/nimg.2002.1131
Uddin LQ (2015) Salience processing and insular cortical function and dysfunction. Nat Rev Neurosci 16(1):55–61. https://doi.org/10.1038/nrn3857
Wu T, Chen C, Spagna A, Wu X, Mackie MA, Russell-Giller S, Xu P, Luo YJ, Liu X, Hof PR, Fan J (2020) The functional anatomy of cognitive control: a domain-general brain network for uncertainty processing. J Comp Neurol 528(8):1265–1292. https://doi.org/10.1002/cne.24804
Yan CG, Wang XD, Zuo XN, Zang YF (2016) DPABI: data processing & analysis for (resting-state) brain imaging. Neuroinformatics 14(3):339–351. https://doi.org/10.1007/s12021-016-9299-4
Acknowledgements
Meng Zhang received support from the National Natural Science Foundation of China (31600927, 81830040), and the Youth Foundation of Social Science and Humanity, China Ministry of Education (21YJC190023). The funders had no role in the study design, data collection, analysis and interpretation of data, writing of the manuscript, or in the decision to submit the article for publication.
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MZ: Conceptualization, Investigation, Writing original draft, and Funding acquisition. YP: Data curation, Methodology, Formal analysis, and Writing–review and editing.
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Zhang, M., Peng, Y. Anterior insula and dorsal anterior cingulate cortex as a hub of self-regulation: combining activation likelihood estimation meta-analysis and meta-analytic connectivity modeling analysis. Brain Struct Funct 228, 1329–1345 (2023). https://doi.org/10.1007/s00429-023-02652-9
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DOI: https://doi.org/10.1007/s00429-023-02652-9