Mean diffusivity of globus pallidus associated with verbal creativity measured by divergent thinking and creativity‐related temperaments in young healthy adults

Recent investigations revealed mean diffusivity (MD) in gray matter and white matter areas is correlated with individual cognitive differences in healthy subjects and show unique properties and sensitivity that other neuroimaging tools donot have. In this study, we tested the hypothesis that the MD in the dopaminergic system is associated with individual differences in verbal creativity measured by divergent thinking (VCDT) and novelty seeking based on prior studies suggesting associations between these and dopaminergic functions. We examined this issue in a large sample of right‐handed healthy young adults. We used analyses of MD and a psychological measure of VCDT, as well as personality measures of the Temperament and Character Inventory (TCI). Our results revealed associations between higher VCDT and lower MD in the bilateral globus pallidus. Furthermore, not only higher novelty seeking, but also lower harm avoidance, higher self‐directedness, and higher self‐transcendence were robustly associated with lower MD in the right globus pallidus, whereas higher persistence was associated with lower MD in the left globus pallidus. These personality variables were also associated with VCDT. The globus pallidus receives the dopaminergic input from the substantia nigra and plays a key role in motivation which is critically linked to dopamine. These results suggested the MD in the globus pallidus, underlie the association between VCDT and multiple personalities in TCI including novelty seeking. Hum Brain Mapp 36:1808–1827, 2015. © 2015 The Authors Human Brain Mapping Published by Wiley Periodicals, Inc.

[1]  Hidenao Fukuyama,et al.  Water diffusion reveals networks that modulate multiregional morphological plasticity after repetitive brain stimulation , 2014, Proceedings of the National Academy of Sciences.

[2]  R. Kawashima,et al.  White matter structures associated with emotional intelligence: Evidence from diffusion tensor imaging , 2013, Human brain mapping.

[3]  Rex E. Jung,et al.  Biochemical Support for the “Threshold” Theory of Creativity: A Magnetic Resonance Spectroscopy Study , 2009, The Journal of Neuroscience.

[4]  R. Kawashima,et al.  Working memory training improves emotional states of healthy individuals , 2014, Front. Syst. Neurosci..

[5]  H. J. Eysenck,et al.  Personality and the Barron-Welsh Art Scale , 1993, Perceptual and motor skills.

[6]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[7]  Yasuyuki Taki,et al.  Regional gray matter volume of dopaminergic system associate with creativity: Evidence from voxel-based morphometry , 2010, NeuroImage.

[8]  A. Cools,et al.  Prepulse inhibition and latent inhibition: the role of dopamine in the medial prefrontal cortex , 1996, Neuroscience.

[9]  E. Esposito,et al.  Serotonin-dopamine interaction: experimental evidence and therapeutic relevance. Preface. , 2008, Progress in brain research.

[10]  Wei Zhang,et al.  Selective aberrant functional connectivity of resting state networks in social anxiety disorder , 2010, NeuroImage.

[11]  Ulrich Ettinger,et al.  Schizotypy, attention deficit hyperactivity disorder, and dopamine genes , 2006, Psychiatry and clinical neurosciences.

[12]  Yasuyuki Taki,et al.  White matter structures associated with creativity: Evidence from diffusion tensor imaging , 2010, NeuroImage.

[13]  Håkon Grydeland,et al.  Social reward dependence and brain white matter microstructure. , 2012, Cerebral cortex.

[14]  Cloninger Cr,et al.  Temperament and personality. , 1994 .

[15]  C. Chiapponi,et al.  Linking novelty seeking and harm avoidance personality traits to basal ganglia: volumetry and mean diffusivity , 2014, Brain Structure and Function.

[16]  L. Chiodo,et al.  Serotonergic afferent regulation of the basic physiology and pharmacological responsiveness of nigrostriatal dopamine neurons. , 1990, The Journal of pharmacology and experimental therapeutics.

[17]  K. Davis,et al.  Two systems of resting state connectivity between the insula and cingulate cortex , 2009, Human brain mapping.

[18]  Y. Benjamini,et al.  Adaptive linear step-up procedures that control the false discovery rate , 2006 .

[19]  S. D. Glick,et al.  Lateral asymmetry of neurotransmitters in human brain , 1982, Brain Research.

[20]  B. Hommel,et al.  The (b)link between creativity and dopamine: Spontaneous eye blink rates predict and dissociate divergent and convergent thinking , 2010, Cognition.

[21]  M S Buchsbaum,et al.  Regional and global changes in cerebral diffusion with normal aging. , 2001, AJNR. American journal of neuroradiology.

[22]  Jordan B. Peterson,et al.  PERSONALITY PROCESSES AND INDIVIDUAL DIFFERENCES Decreased Latent Inhibition Is Associated With Increased Creative Achievement in High-Functioning Individuals , 2003 .

[23]  J. Raven,et al.  Manual for Raven's progressive matrices and vocabulary scales , 1962 .

[24]  H. Akaike A new look at the statistical model identification , 1974 .

[25]  Hiroshi Fukuda,et al.  Correlation among body height, intelligence, and brain gray matter volume in healthy children , 2012, NeuroImage.

[26]  Yasuyuki Taki,et al.  The association between resting functional connectivity and creativity. , 2012, Cerebral cortex.

[27]  Yasuyuki Taki,et al.  Failing to deactivate: The association between brain activity during a working memory task and creativity , 2011, NeuroImage.

[28]  Jarmo Hietala,et al.  Personality traits and striatal dopamine synthesis capacity in healthy subjects. , 2003, The American journal of psychiatry.

[29]  S. Cooper Changing Notions of Defense Within Psychoanalytic Theory , 1998 .

[30]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[31]  Kenneth M. Heilman,et al.  Cortical morphology of visual creativity , 2011, Neuropsychologia.

[32]  Ignacio González Burgos,et al.  Serotonin-dopamine interaction: experimental evidence and therapeutic relevance , 2009 .

[33]  Yasuyuki Taki,et al.  Training of Working Memory Impacts Structural Connectivity , 2010, The Journal of Neuroscience.

[34]  Juha O. Rinne,et al.  Personality traits and brain dopaminergic function in Parkinson's disease , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Jianju Liu,et al.  Regional diffusion changes of cerebral grey matter during normal aging--a fluid-inversion prepared diffusion imaging study. , 2010, European journal of radiology.

[36]  J. Guilford,et al.  The nature of human intelligence. , 1968 .

[37]  T. Kitamura,et al.  Reliability and Validity of the Japanese Version of the Temperament and Character Inventory , 2000, Psychological reports.

[38]  S. Haber,et al.  The cortico-basal ganglia integrative network: The role of the thalamus , 2009, Brain Research Bulletin.

[39]  Richard P. Bentall,et al.  Schizotypy and creativity: an evolutionary connection? , 2001 .

[40]  R. Haier,et al.  White Matter Integrity, Creativity, and Psychopathology: Disentangling Constructs with Diffusion Tensor Imaging , 2010, PloS one.

[41]  Semir Zeki,et al.  Neural Correlates of Hate , 2008, PloS one.

[42]  Hiroshi Fukuda,et al.  Correlation between gray matter density‐adjusted brain perfusion and age using brain MR images of 202 healthy children , 2011, Human brain mapping.

[43]  Yasuyuki Taki,et al.  Working Memory Training Using Mental Calculation Impacts Regional Gray Matter of the Frontal and Parietal Regions , 2011, PloS one.

[44]  K. Heilman,et al.  Creative Innovation: Possible Brain Mechanisms , 2003, Neurocase.

[45]  Sheri J. Broyles,et al.  Creativity and the Five-Factor Model , 1996 .

[46]  M. Kawato,et al.  Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. , 2006, Journal of neurophysiology.

[47]  A. Flaherty Frontotemporal and dopaminergic control of idea generation and creative drive , 2005, The Journal of comparative neurology.

[48]  Edward M. Bowden,et al.  Neural Activity When People Solve Verbal Problems with Insight , 2004, PLoS biology.

[49]  Ramon Casanova,et al.  Biological parametric mapping: A statistical toolbox for multimodality brain image analysis , 2007, NeuroImage.

[50]  I. Törk Anatomy of the Serotonergic System a , 1990, Annals of the New York Academy of Sciences.

[51]  Y. Assaf,et al.  Diffusion Tensor Imaging (DTI)-based White Matter Mapping in Brain Research: A Review , 2007, Journal of Molecular Neuroscience.

[52]  R. Haier,et al.  Neuroanatomy of creativity , 2009, Human brain mapping.

[53]  Yasuyuki Taki,et al.  Regional gray matter density associated with emotional intelligence: Evidence from voxel‐based morphometry , 2011, Human brain mapping.

[54]  M. Hansenne,et al.  Relationships between Cloninger's biosocial model of personality and the behavioral inhibition/approach systems (BIS/BAS) , 2007 .

[55]  D. Levine,et al.  A neuropsychological theory of positive affect and its influence on cognition. , 1999, Psychological review.

[56]  Benjamin Thyreau,et al.  White matter structures associated with empathizing and systemizing in young adults , 2013, NeuroImage.

[57]  A. Stefani,et al.  Magnetic resonance imaging markers of Parkinson's disease nigrostriatal signature. , 2010, Brain : a journal of neurology.

[58]  T Watanabe [A study on the individual differences of the experience of hypnagogic imagery]. , 1998, Shinrigaku kenkyu : The Japanese journal of psychology.

[59]  A. Björklund,et al.  Dopaminergic innervation of the globus pallidus by collaterals from the nigrostriatal pathway , 1979, Brain Research.

[60]  Kyung Hee Kim,et al.  Meta‐Analyses of the Relationship of Creative Achievement to Both IQ and Divergent Thinking Test Scores , 2008 .

[61]  M. Lorr,et al.  Profile of mood states , 1971 .

[62]  Yasuyuki Taki,et al.  Regional gray and white matter volume associated with Stroop interference: Evidence from voxel-based morphometry , 2012, NeuroImage.

[63]  J. Aharon-Peretz,et al.  Novelty seeking and harm avoidance in Parkinson’s disease: effects of asymmetric dopamine deficiency , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[64]  Jin Fan,et al.  Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies , 2011, Neuroscience & Biobehavioral Reviews.

[65]  C. R. Cloninger,et al.  A unified biosocial theory of personality and its role in the development of anxiety states. , 1986, Psychiatric developments.

[66]  Kjell Någren,et al.  Insular dopamine D2 receptors and novelty seeking personality in Parkinson's disease , 2004, Movement disorders : official journal of the Movement Disorder Society.

[67]  J. Illes,et al.  Diffusion-tensor imaging of cognitive performance , 2002, Brain and Cognition.

[68]  Anders M. Fjell,et al.  A multi-modal investigation of behavioral adjustment: Post-error slowing is associated with white matter characteristics , 2012, NeuroImage.

[69]  Qinglin Zhang,et al.  Relating Inter-Individual Differences in Verbal Creative Thinking to Cerebral Structures: An Optimal Voxel-Based Morphometry Study , 2013, PloS one.

[70]  Pierre-Yves Oudeyer,et al.  In Search of the Neural Circuits of Intrinsic Motivation , 2007, Front. Neurosci..

[71]  K M Heilman,et al.  Motor dominance and lateral asymmetry of the globus pallidus , 1988, Neurology.

[72]  M. Csíkszentmihályi Creativity: Flow and the Psychology of Discovery and Invention , 1996 .

[73]  C. R. Cloninger,et al.  Temperament and personality , 1994, Current Opinion in Neurobiology.

[74]  Werner Jaschke,et al.  Comparison of diffusion‐weighted imaging and [123I]IBZM‐SPECT for the differentiation of patients with the Parkinson variant of multiple system atrophy from those with Parkinson's disease , 2004, Movement disorders : official journal of the Movement Disorder Society.

[75]  J. Kulisevsky,et al.  Changes in artistic style and behaviour in Parkinson’s disease: dopamine and creativity , 2009, Journal of Neurology.

[76]  A. Kramer,et al.  Be smart, exercise your heart: exercise effects on brain and cognition , 2008, Nature Reviews Neuroscience.

[77]  P. Kline,et al.  Psychoticism and creativity. , 1986, The Journal of genetic psychology.

[78]  C Barbui,et al.  Cortical white-matter microstructure in schizophrenia. Diffusion imaging study. , 2007, The British journal of psychiatry : the journal of mental science.

[79]  Yasuyuki Taki,et al.  Verbal working memory performance correlates with regional white matter structures in the frontoparietal regions , 2011, Neuropsychologia.

[80]  K. Heilman,et al.  Creativity in Parkinson's disease as a function of right versus left hemibody onset , 2009, Journal of the Neurological Sciences.

[81]  C. A. Clark,et al.  A structural equation modeling investigation of age-related variance in executive function and DTI measured white matter damage , 2008, Neurobiology of Aging.

[82]  Yasuyuki Taki,et al.  Effects of Training of Processing Speed on Neural Systems , 2011, The Journal of Neuroscience.

[83]  Yoshiro Okubo,et al.  Dopamine D2 Receptors in the Insular Cortex and the Personality Trait of Novelty Seeking , 2001, NeuroImage.

[84]  C. Robert Cloninger,et al.  Psychometric Properties of the Temperament and Character Inventory–Revised (TCI–R) in a Belgian Sample , 2005, Journal of personality assessment.

[85]  Yasuyuki Taki,et al.  Cerebral Blood Flow during Rest Associates with General Intelligence and Creativity , 2011, PloS one.

[86]  Ilona Papousek,et al.  Gray matter density in relation to different facets of verbal creativity , 2013, Brain Structure and Function.

[87]  Yasuyuki Taki,et al.  The correlation between brain gray matter volume and empathizing and systemizing quotients in healthy children , 2012, NeuroImage.

[88]  R. Kawashima,et al.  Linear and curvilinear correlations of brain white matter volume, fractional anisotropy, and mean diffusivity with age using voxel‐based and region‐of‐interest analyses in 246 healthy children , 2013, Human brain mapping.

[89]  Ryuta Kawashima,et al.  Effects of processing speed training on cognitive functions and neural systems , 2012, Reviews in the neurosciences.

[90]  Laura Petrosini,et al.  New evidence for the cerebellar involvement in personality traits , 2013, Front. Behav. Neurosci..

[91]  J. Lépine,et al.  Normative data and factor structure of the Temperament and Character Inventory (TCI) in the French version , 2000, Psychiatry Research.

[92]  D. Le Bihan,et al.  Diffusion tensor imaging: Concepts and applications , 2001, Journal of magnetic resonance imaging : JMRI.

[93]  Seiki Tajima,et al.  Personality traits associated with intrinsic academic motivation in medical students , 2009, Medical education.

[94]  R. Ebstein,et al.  The association between creativity and 7R polymorphism in the dopamine receptor D4 gene (DRD4) , 2013, Front. Hum. Neurosci..

[95]  K. Nakazato,et al.  Creativity and Factors Affecting Creative Ability in Adulthood and Old Age , 2007 .

[96]  Neal R. Swerdlow,et al.  Dopamine agonists disrupt visual latent inhibition in normal males using a within-subject paradigm , 2003, Psychopharmacology.

[97]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[98]  Joseph A Maldjian,et al.  Precentral gyrus discrepancy in electronic versions of the Talairach atlas , 2004, NeuroImage.

[99]  R. Depue,et al.  Neurobiology of the structure of personality: Dopamine, facilitation of incentive motivation, and extraversion , 1999, Behavioral and Brain Sciences.

[100]  G. Rees,et al.  The structural basis of inter-individual differences in human behaviour and cognition , 2011, Nature Reviews Neuroscience.

[101]  Y. Goshima,et al.  Differential neurotoxicity induced by l-DOPA and dopamine in cultured striatal neurons , 1996, Brain Research.

[102]  B. Hommel,et al.  More creative through positive mood? Not everyone! , 2012, Front. Hum. Neurosci..

[103]  J. Blau Color Atlas of Neuroscience. Neuroanatomy and Neurophysiology , 2000 .

[104]  C. Jack,et al.  Mild cognitive impairment and Alzheimer disease: regional diffusivity of water. , 2001, Radiology.

[105]  W. Sauser,et al.  Creativity and Certain Personality Traits: Understanding the Mediating Effect of Intrinsic Motivation , 2008 .

[106]  C. R. Cloninger,et al.  A psychobiological model of temperament and character. , 1993, Archives of general psychiatry.

[107]  M. Horino,et al.  THE EFFECTS OF ACHIEVEMENT MOTIVATION ON RELATIONSHIPS BETWEEN DEPRESSION AND SOCIAL SUPPORT , 1991 .

[108]  Benjamin Thyreau,et al.  Sleep duration during weekdays affects hippocampal gray matter volume in healthy children , 2012, NeuroImage.

[109]  Michael Davidson,et al.  Serotonin, dopamine and their interactions in schizophrenia , 1993, Psychopharmacology.

[110]  R. Kawashima,et al.  Regional gray matter density is associated with achievement motivation: evidence from voxel-based morphometry , 2012, Brain Structure and Function.

[111]  T. Klingberg,et al.  Prefrontal cortex and basal ganglia control access to working memory , 2008, Nature Neuroscience.

[112]  Carolyn C. Meltzer,et al.  Increased Dopamine D2/D3 Receptor Binding After Recovery from Anorexia Nervosa Measured by Positron Emission Tomography and [11C]Raclopride , 2005, Biological Psychiatry.

[113]  F. Piras,et al.  Working memory performance and thalamus microstructure in healthy subjects , 2010, Neuroscience.

[114]  Ahmed Abdel Khalek Abdel Razek,et al.  Idiopathic Parkinson disease effect of levodopa on apparent diffusion coefficient value of the brain. , 2011, Academic radiology.

[115]  Yaniv Assaf,et al.  Learning in the Fast Lane: New Insights into Neuroplasticity , 2012, Neuron.

[116]  Kangcheng Wang,et al.  Increased resting functional connectivity of the medial prefrontal cortex in creativity by means of cognitive stimulation , 2014, Cortex.

[117]  L. Siever,et al.  New perspectives on schizotypal personality disorder , 2000, Current psychiatry reports.

[118]  Cloninger Cr Discussions arising from: Cloninger, CR. A. unified biosocial theory of personality and its role in the development of anxiety states. , 1987, Psychiatric developments.

[119]  Rosa Aurora Chavez-Eakle,et al.  Personality: A Possible Bridge Between Creativity and Psychopathology? , 2006 .

[120]  Zang-Hee Cho,et al.  Association of harm avoidance with dopamine D2/3 receptor availability in striatal subdivisions: A high resolution PET study , 2011, Biological Psychology.

[121]  F. Crawford,et al.  DRD4 and novelty seeking: results of meta-analyses. , 2002, American journal of medical genetics.

[122]  M. Gluck,et al.  Reward-learning and the novelty-seeking personality: a between- and within-subjects study of the effects of dopamine agonists on young Parkinson's patients. , 2009, Brain : a journal of neurology.

[123]  A. Dietrich,et al.  Who's afraid of a cognitive neuroscience of creativity? , 2007, Methods.

[124]  F. Yasuno,et al.  Relation among dopamine D2 receptor binding, obesity and personality in normal human subjects , 2001, Neuroscience Letters.

[125]  Yasuyuki Taki,et al.  Association of hair iron levels with creativity and psychological variables related to creativity , 2013, Front. Hum. Neurosci..

[126]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.