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Subcortical structures and visual divergent thinking: a resting-state functional MRI analysis

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Abstract

An increasing number of studies have found that a few, specific subcortical regions are involved in creative visual divergent thinking. In addition, creative thinking is heavily reliant on the fronto-striatal dopaminergic pathways. This study aimed to explore whether spontaneous fluctuations in the subcortex, which contribute to our creative abilities, showed significant differences between individuals with different levels of creativity based on resting-state functional magnetic resonance imaging data. We calculated subcortical regions’ seed-wise and dynamic functional connectivity (dFC), and then examined the differences between the high and low visual creativity groups. Furthermore, the topological properties of the subcortical network were measured, and their relationship with creative visual divergent thinking was calculated using brain–behavior correlation analyses. The results showed that functional connectivity (FC) between the putamen, pallidum, and thalamus indicated group differences within the subcortex. Whole-brain FC results showed group differences across subcortical (i.e., the thalamus and pallidum) and cerebral regions (i.e., the insula, middle frontal gyrus, and middle temporal gyrus). In addition, subcortical FC demonstrated a positive correlation with visual divergent thinking scores across the pallidum, putamen, and thalamus. Our findings provide novel insights into the relationship between visual divergent thinking and the activities of the subcortex. It is likely that not only fronto-striatal dopaminergic pathways, but also “motor” pathways, are involved in creative visual divergent thinking processing.

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References

  • Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381

    Article  CAS  Google Scholar 

  • Alexander GE, Crutcher MD, DeLong MR (1990) Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, prefrontal and limbic functions. Prog Brain Res 85:119–146

    Article  CAS  PubMed  Google Scholar 

  • Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD (2014) Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex 24:663–676

    Article  PubMed  Google Scholar 

  • Ashby FG, Isen AM, Turken AU (1999) A neuropsychological theory of positive affect and its influence on cognition. Psychol Rev 106:529–550

    Article  CAS  PubMed  Google Scholar 

  • Aston-Jones G, Cohen JD (2005) An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 28:403–450

    Article  CAS  PubMed  Google Scholar 

  • Baas M, Roskes M, Sligte D, Nijstad BA, De Dreu CK (2013) Personality and creativity: the dual pathway to creativity model and a research agenda. Soc Pers Psychol Compass 7:732–748

    Article  Google Scholar 

  • Baliki MN, Mansour A, Baria AT, Huang LJ, Berger SE, Fields HL, Apkarian AV (2013) Parceling human accumbens into putative core and shell dissociates encoding of values for reward and pain. J Neurosci 33:16383–16393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beaty RE, Benedek M, Kaufman SB, Silvia PJ (2015) Default and executive network coupling supports creative idea production. Sci Rep 5:10964

    Article  PubMed  PubMed Central  Google Scholar 

  • Benedek M, Beaty R, Jauk E, Koschutnig K, Fink A, Silvia PJ, Dunst B, Neubauer AC (2014) Creating metaphors: the neural basis of figurative language production. Neuroimage 90:99–106

    Article  PubMed  Google Scholar 

  • Berridge CW, Waterhouse BD (2003) The locus coeruleus–noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Rev 42:33–84

    Article  PubMed  Google Scholar 

  • Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541

    Article  CAS  PubMed  Google Scholar 

  • Boot N, Baas M, van Gaal S, Cools R, De Dreu CK (2017) Creative cognition and dopaminergic modulation of fronto-striatal networks: Integrative review and research agenda. Neurosci Biobehav Rev 78:13–23

    Article  CAS  PubMed  Google Scholar 

  • Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198

    Article  CAS  PubMed  Google Scholar 

  • Cajal SR (1995) Histology of the nervous system of man and vertebrates, vol 1. Oxford University Press, Oxford

    Google Scholar 

  • Calhoun VD, Miller R, Pearlson G, Adalı T (2014) The chronnectome: time-varying connectivity networks as the next frontier in fMRI data discovery. Neuron 84:262–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chávez-Eakle RA, Graff-Guerrero A, García-Reyna JC, Vaugier V, Cruz-Fuentes C (2007) Cerebral blood flow associated with creative performance: a comparative study. Neuroimage 38:519–528

    Article  PubMed  Google Scholar 

  • Chen Q, Beaty RE, Cui Z, Sun J, He H, Zhuang K, Ren Z, Liu G, Qiu J (2019) Brain hemispheric involvement in visuospatial and verbal divergent thinking. Neuroimage 202:116065

    Article  PubMed  Google Scholar 

  • Chermahini SA, Hommel B (2010) The (b)link between creativity and dopamine: spontaneous eye blink rates predict and dissociate divergent and convergent thinking. Cognition 115:458–465

    Article  PubMed  Google Scholar 

  • Cohen J (2013) Statistical power analysis for the behavioral sciences. Routledge Academic, London

    Book  Google Scholar 

  • De Dreu CKW, Baas M, Roskes M, Sligte DJ, Ebstein RP, Chew SH, Tong T, Jiang Y, Mayseless N, Shamay-Tsoory SG (2014) Oxytonergic circuitry sustains and enables creative cognition in humans. Soc Cogn Affect Neurosci 9:1159–1165

    Article  PubMed  Google Scholar 

  • De Dreu CKW, Kret ME (2016) Oxytocin conditions intergroup relations through upregulated in-group empathy, cooperation, conformity, and defense. Biol Psychiatry 79:165–173

    Article  PubMed  CAS  Google Scholar 

  • de Manzano Ö, Ullén F (2012) Goal-independent mechanisms for free response generation: Creative and pseudo-random performance share neural substrates. Neuroimage 59:772–780

    Article  PubMed  Google Scholar 

  • De Manzano Ö, Cervenka S, Karabanov A, Farde L, Ullen F (2010) Thinking outside a less intact box: thalamic dopamine D2 receptor densities are negatively related to psychometric creativity in healthy individuals. PLoS ONE 5:e10670

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dietrich A, Kanso R (2010) A review of EEG, ERP, and neuroimaging studies of creativity and insight. Psychol Bull 136:822

    Article  PubMed  Google Scholar 

  • Faust-Socher A, Kenett YN, Cohen OS, Hassin-Baer S, Inzelberg R (2014) Enhanced creative thinking under dopaminergic therapy in Parkinson disease. Annals Neurol 75:935–942

    Article  CAS  Google Scholar 

  • Fink A, Benedek M, Koschutnig K, Papousek I, Weiss EM, Bagga D, Schöpf V (2018) Modulation of resting-state network connectivity by verbal divergent thinking training. Brain Cogn 128:1–6

    Article  PubMed  Google Scholar 

  • Gao Z, Zhang D, Liang A, Liang B, Wang Z, Cai Y, Li J, Gao M, Jiao B, Huang R, Liu M (2017) Exploring the associations between intrinsic brain connectivity and creative ability using functional connectivity strength and connectome analysis. Brain Connectivity 7:590–601

    Article  PubMed  Google Scholar 

  • Heilman KM, Nadeau SE, Beversdorf DO (2003) Creative innovation: possible brain mechanisms. Neurocase 9:369–379

    Article  PubMed  Google Scholar 

  • Hutchison RM, Womelsdorf T, Gati JS, Everling SM, Ravi S (2013) Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques. Hum Brain Mapp 34:2154–2177

    Article  PubMed  Google Scholar 

  • Kenett YN, Betzel RF, Beaty RE (2020) Community structure of the creative brain at rest. Neuroimage 210:116578

    Article  PubMed  Google Scholar 

  • Kounios J, Fleck JI, Green DL, Payne L, Stevenson JL, Bowden EM, Jung-Beeman M (2008) The origins of insight in resting-state brain activity. Neuropsychologia 46:281–291

    Article  PubMed  Google Scholar 

  • Kowatari Y, Lee SH, Yamamura H, Nagamori Y, Levy P, Yamane S, Yamamoto M (2009) Neural networks involved in artistic creativity. Hum Brain Mapp 30:1678–1690

    Article  PubMed  Google Scholar 

  • Liao W, Wu G-R, Xu Q, Ji G-J, Zhang Z, Zang Y-F et al (2014) DynamicBC: a MATLAB toolbox for dynamic brain connectome analysis. Brain Connectivity 4(10):780–790

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahler SV, Berridge KC (2011) What and when to “want”? Amygdala-based focusing of incentive salience upon sugar and sex. Psychopharmacology 221:407–426

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Marusak HA, Calhoun VD, Brown S, Crespo LM, Sala-Hamrick K, Gotlib IH, Thomason ME (2017) Dynamic functional connectivity of neurocognitive networks in children. Hum Brain Mapp 38:97–108

    Article  PubMed  Google Scholar 

  • Mayseless N, Shamay-Tsoory SG (2015) Enhancing verbal creativity: modulating creativity by altering the balance between right and left inferior frontal gyrus with tDCS. Neuroscience 291:167–176

    Article  CAS  PubMed  Google Scholar 

  • Mayseless N, Uzefovsky F, Shalev I, Ebstein RP, Shamay-Tsoory SG (2013) The association between creativity and 7R polymorphism in the dopamine receptor D4 gene (DRD4). Front Hum Neurosci 7:502

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Navalpotro-Gomez I, Kim J, Paz-Alonso PM, Delgado-Alvarado M, Quiroga-Varela A, Jimenez-Urbieta H, Carreiras M, Strafella AP, Rodriguez-Oroz MC (2020) Disrupted salience network dynamics in Parkinson’s disease patients with impulse control disorders. Parkinsonism Relat Disord 70:74–81

    Article  PubMed  Google Scholar 

  • Patil AU, Ghate S, Madathil D, Tzeng OJL, Huang H-W, Huang C-M (2021) Static and dynamic functional connectivity supports the configuration of brain networks associated with creative cognition. Sci Rep 11:1–17

    Article  CAS  Google Scholar 

  • Peterson JB, Smith KW, Carson S (2002) Openness and extraversion are associated with reduced latent inhibition: replication and commentary. Pers Individ Differ 33:1137–1147

    Article  Google Scholar 

  • Pinho AL, Ullén F, Castelo-Branco M, Fransson P, de Manzano Ö (2015) Addressing a paradox: dual strategies for creative performance in introspective and extrospective networks. Cereb Cortex 26:3052–3063

    Article  PubMed  Google Scholar 

  • Puglisi-Allegra S, Ventura R (2012) Prefrontal/accumbal catecholamine system processes high motivational salience. Front Behav Neurosci 6:31

    Article  PubMed  PubMed Central  Google Scholar 

  • Rashid B, Arbabshirani MR, Damaraju E, Cetin MS, Miller R, Pearlson GD, Calhoun VD (2016) Classification of schizophrenia and bipolar patients using static and dynamic resting-state fMRI brain connectivity. Neuroimage 134:645–657

    Article  PubMed  Google Scholar 

  • Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069

    Article  PubMed  Google Scholar 

  • Salvi C, Bricolo E, Franconeri SL, Kounios J, Beeman M (2015) Sudden insight is associated with shutting out visual inputs. Psychon Bull Rev 22:1814–1819

    Article  PubMed  Google Scholar 

  • Schuler AL, Tik M, Sladky R, Luft CDB, Hoffmann A, Woletz M, Zioga I, Bhattacharya J, Windischberger C (2019) Modulations in resting state networks of subcortical structures linked to creativity. Neuroimage 195:311–319

    Article  PubMed  Google Scholar 

  • Shen W, Tong Y, Li F, Yuan Y, Hommel B, Liu C, Luo J (2018) Tracking the neurodynamics of insight: a meta-analysis of neuroimaging studies. Biol Psychol 138:189–198

    Article  PubMed  Google Scholar 

  • Sokoloff L, Wechsler RL, Mangold R, Balls K, Kety SS (1953) Cerebral blood flow and oxygen consumption in hyperthyroidism before and after treatment. J Clin Investig 32:202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strogatz SH (2001) Exploring complex networks. Nature 410:268–276

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Zhang Q, Li Y, Meng J, Chen Q, Yang W, Wei D, Qiu J (2020) Plasticity of the resting-state brain: static and dynamic functional connectivity change induced by divergent thinking training. Brain Imaging Behav 14:1498–1506

    Article  PubMed  Google Scholar 

  • Sweitzer MM, Kollins SH, Kozink RV, Hallyburton M, English J, Addicott MA, Oliver JA, McClernon FJ (2018) ADHD, smoking withdrawal, and inhibitory control: results of a neuroimaging study with methylphenidate challenge. Neuropsychopharmacology 43:851

    Article  PubMed  Google Scholar 

  • Takeuchi H, Taki Y, Sassa Y, Hashizume H, Sekiguchi A, Fukushima A, Kawashima R (2010) Regional gray matter volume of dopaminergic system associate with creativity: evidence from voxel-based morphometry. Neuroimage 51:578–585

    Article  PubMed  Google Scholar 

  • Thelen E, Schöner G, Scheier C, Smith LB (2001) The dynamics of embodiment: a field theory of infant perseverative reaching. Behav Brain Sci 24:1–34

    Article  CAS  PubMed  Google Scholar 

  • Tik M, Sladky R, Luft CDB, Willinger D, Hoffmann A, Banissy MJ, Bhattacharya J, Windischberger C (2018) Ultra-high-field fMRI insights on insight: neural correlates of the Aha!-moment. Hum Brain Mapp 39:3241–3252

    Article  PubMed  PubMed Central  Google Scholar 

  • Torrance EP (1990) Torrance tests of creative thinking. Figural forms A and B: directions manual. Scholastic testing service

  • Wang J-H, Zuo X-N, Gohel S, Milham MP, Biswal BB, He Y (2011) Graph theoretical analysis of functional brain networks: test-retest evaluation on short-and long-term resting-state functional MRI data. PLoS ONE 6:e21976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wei D, Yang J, Li W, Wang K, Zhang Q, Qiu J (2014) Increased resting functional connectivity of the medial prefrontal cortex in creativity by means of cognitive stimulation. Cortex 51:92–102

    Article  PubMed  Google Scholar 

  • Wenzel JM, Rauscher NA, Cheer JF, Oleson EB (2015) A role for phasic dopamine release within the nucleus accumbens in encoding aversion: a review of the neurochemical literature. ACS Chem Neurosci 6:16–26

    Article  CAS  PubMed  Google Scholar 

  • Willeit M, Popovic A, Bartova L, Sauerzopf U, Bauer M, Praschak-Rieder N (2016) In vivo imaging of dopamine metabolism and dopamine transporter function in the human brain. Neurotransmitter transporters. Humana Press, New York, pp 203–220

    Chapter  Google Scholar 

  • Yan CG, Zang Y-F (2010) DPARSF: a MATLAB toolbox for pipeline data analysis of resting-state fMRI. Front Syst Neurosci 4:1–7

    Google Scholar 

  • Yan C, Cheung B, Kelly C, Colcombe S, Craddock RC, Di Martino A, Li Q, Zuo X, Castellanos FX, Milham MP (2013) A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. Neuroimage 76:183–201

    Article  PubMed  Google Scholar 

  • Zabelina DL, Colzato L, Beeman M, Hommel B (2016) Dopamine and the creative mind: Individual differences in creativity are predicted by interactions between dopamine genes DAT and COMT. PLoS ONE 11:e046768

    Article  CAS  Google Scholar 

  • Zou Q, Ross TJ, Gu H, Geng X, Zuo XN, Hong LE, Gao J-H, Stein EA, Zang Y-F, Yang Y (2013) Intrinsic resting-state activity predicts working memory brain activation and behavioral performance. Hum Brain Mapp 34:3204–3215

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was sponsored by the ECNU Academic Innovation Promotion Program for Excellent Doctoral Students (YBNLTS2019-027) to ZG.

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ZG, XL, DZ, ML, and NH conceived the experiment. ZG, XL, and DZ performed the research. XL, and ZG analyzed the data. ZG, XL, and NH wrote the paper.

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Correspondence to Ning Hao.

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Gao, Z., Liu, X., Zhang, D. et al. Subcortical structures and visual divergent thinking: a resting-state functional MRI analysis. Brain Struct Funct 226, 2617–2627 (2021). https://doi.org/10.1007/s00429-021-02355-z

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