Grapheme-color synesthetes show peculiarities in their emotional brain: cortical and subcortical evidence from VBM analysis of 3D-T1 and DTI data

Grapheme-color synesthesia is a neurological phenomenon in which viewing achromatic letters/numbers leads to automatic and involuntary color experiences. In this study, voxel-based morphometry analyses were performed on T1 images and fractional anisotropy measures to examine the whole brain in associator grapheme-color synesthetes. These analyses provide new evidence of variations in emotional areas (both at the cortical and subcortical levels), findings that help understand the emotional component as a relevant aspect of the synesthetic experience. Additionally, this study replicates previous findings in the left intraparietal sulcus and, for the first time, reports the existence of anatomical differences in subcortical gray nuclei of developmental grapheme-color synesthetes, providing a link between acquired and developmental synesthesia. This empirical evidence, which goes beyond modality-specific areas, could lead to a better understanding of grapheme-color synesthesia as well as of other modalities of the phenomenon.

[1]  Karsten Specht,et al.  An independent component analysis of fMRI data of grapheme-colour synaesthesia. , 2011, Journal of neuropsychology.

[2]  G. Bargary,et al.  Synaesthesia and cortical connectivity , 2008, Trends in Neurosciences.

[3]  Gregory McCarthy,et al.  Emotion-attention network interactions during a visual oddball task. , 2004, Brain research. Cognitive brain research.

[4]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[5]  F. Varela,et al.  Radical embodiment: neural dynamics and consciousness , 2001, Trends in Cognitive Sciences.

[6]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

[7]  Tony Ro,et al.  Neural Substrates of Sound–Touch Synesthesia after a Thalamic Lesion , 2008, The Journal of Neuroscience.

[8]  Duane E. Haines,et al.  Neuroanatomy : an atlas of structures, sections, and , 2008 .

[9]  Gereon R Fink,et al.  Grapheme-colour synaesthetes show increased grey matter volumes of parietal and fusiform cortex. , 2009, Brain : a journal of neurology.

[10]  Romke Rouw,et al.  Neural Basis of Individual Differences in Synesthetic Experiences , 2010, The Journal of Neuroscience.

[11]  Jingjing Lu,et al.  Evaluation of Multiple Voxel-Based Morphometry Approaches and Applications in the Analysis of White Matter Changes in Temporal Lobe Epilepsy , 2013, AE-CAI.

[12]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[13]  Corinne E. Fischer,et al.  “Blue is music to my ears”: Multimodal synesthesias after a thalamic stroke , 2012, Neurocase.

[14]  Lutz Jäncke,et al.  The multiple synaesthete E.S. — Neuroanatomical basis of interval-taste and tone-colour synaesthesia , 2008, NeuroImage.

[15]  Jamie Ward,et al.  Emotionally mediated synaesthesia , 2004, Cognitive neuropsychology.

[16]  V. Ramachandran,et al.  Psychophysical investigations into the neural basis of synaesthesia , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[17]  Stefan Gazdzinski,et al.  Cerebral white matter recovery in abstinent alcoholics--a multimodality magnetic resonance study. , 2010, Brain : a journal of neurology.

[18]  W. Singer,et al.  Neuronal Correlates of Colour-Graphemic Synaesthesia: Afmri Study , 2006, Cortex.

[19]  R. Cytowič Touching Tastes, Seeing Smells—and Shaking up Brain Science What Defines Synesthesia? Involuntary and Automatic , 2003 .

[20]  D. N. Pandya,et al.  Insular interconnections with the amygdala in the rhesus monkey , 1981, Neuroscience.

[21]  J. B. Angevine,et al.  The Human Brain in Photographs and Diagrams , 2013 .

[22]  D. Maurer,et al.  Synesthesia: a new approach to understanding the development of perception. , 2013, Developmental psychology.

[23]  V. Ramachandran,et al.  Synaesthesia? A window into perception, thought and language , 2001 .

[24]  P. Whitaker-Azmitia Serotonin and development , 2020, Handbook of Behavioral Neuroscience.

[25]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[26]  John D E Gabrieli,et al.  Bottom-Up and Top-Down Processes in Emotion Generation , 2009, Psychological science.

[27]  Osamu Abe,et al.  Utilization of diffusion tensor tractography in combination with spatial normalization to assess involvement of the corticospinal tract in capsular/pericapsular stroke: Feasibility and clinical implications , 2007, Journal of magnetic resonance imaging : JMRI.

[28]  C. Allen The Human Brain: in photographs and diagrams , 1995 .

[29]  C. Blakemore,et al.  Synaesthetic perception of colour and visual space in a blind subject: An fMRI case study , 2012, Consciousness and Cognition.

[30]  M. Bradley,et al.  Neuroanatomical correlates of pleasant and unpleasant emotion , 1997, Neuropsychologia.

[31]  T. Paus,et al.  Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis , 2000, Experimental Brain Research.

[32]  D. Eagleman,et al.  A standardized test battery for the study of synesthesia , 2007, Journal of Neuroscience Methods.

[33]  P. Hagoort,et al.  Behavioral/systems/cognitive Effective Connectivity Determines the Nature of Subjective Experience in Grapheme-color Synesthesia , 2022 .

[34]  Ivan Toni,et al.  Associating Colours with People: A Case of Chromatic-Lexical Synaesthesia , 2001, Cortex.

[35]  David Brang,et al.  The cross-activation theory at 10. , 2011, Journal of neuropsychology.

[36]  Lynn C. Robertson,et al.  Attenuating illusory binding with TMS of the right parietal cortex , 2007, NeuroImage.

[37]  Timothy Edward John Behrens,et al.  Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. , 2005, Cerebral cortex.

[38]  Anina N. Rich,et al.  Neural correlates of imagined and synaesthetic colours , 2006, Neuropsychologia.

[39]  I. Olson,et al.  The Enigmatic temporal pole: a review of findings on social and emotional processing. , 2007, Brain : a journal of neurology.

[40]  Juan Lupiáñez,et al.  Green love is ugly: Emotions elicited by synesthetic grapheme-color perceptions , 2007, Brain Research.

[41]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[42]  R. Maddock The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain , 1999, Trends in Neurosciences.

[43]  D. Eagleman,et al.  Wednesday Is Indigo Blue: Discovering the Brain of Synesthesia , 2009 .

[44]  Michel Dojat,et al.  The neural bases of grapheme-color synesthesia are not localized in real color-sensitive areas. , 2012, Cerebral cortex.

[45]  Derek K. Jones,et al.  The effect of filter size on VBM analyses of DT-MRI data , 2005, NeuroImage.

[46]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[47]  Olaf Sporns,et al.  Symbiotic relationship between brain structure and dynamics , 2009, BMC Neuroscience.

[48]  Sofia Tsouli,et al.  Psychopharmacology of synesthesia; the role of serotonin S2a receptor activation , 2007 .

[49]  Beat Meier,et al.  Parieto-occipital suppression eliminates implicit bidirectionality in grapheme-colour synaesthesia , 2010, Neuropsychologia.

[50]  Edward M. Hubbard,et al.  Neurophysiology of synesthesia , 2007, Current psychiatry reports.

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

[52]  Shan Shen,et al.  VBM lesion detection depends on the normalization template: a study using simulated atrophy. , 2007, Magnetic resonance imaging.

[53]  Lutz Jäncke,et al.  Globally Altered Structural Brain Network Topology in Grapheme-Color Synesthesia , 2011, The Journal of Neuroscience.

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

[55]  H. Scholte,et al.  Increased structural connectivity in grapheme-color synesthesia , 2007, Nature Neuroscience.

[56]  Gereon R. Fink,et al.  When visual perception causes feeling: Enhanced cross-modal processing in grapheme-color synesthesia , 2005, NeuroImage.

[57]  M. Naumer,et al.  Touching sounds: thalamocortical plasticity and the neural basis of multisensory integration. , 2009, Journal of neurophysiology.

[58]  M. Ríos,et al.  The striatum beyond reward: caudate responds intensely to unpleasant pictures , 2009, Neuroscience.

[59]  Geoffrey M. Boynton,et al.  Individual Differences among Grapheme-Color Synesthetes: Brain-Behavior Correlations , 2005, Neuron.

[60]  Vincent Walsh,et al.  Disruption of synaesthesia following TMS of the right posterior parietal cortex , 2007, Neuropsychologia.

[61]  Zhendong Niu,et al.  Learning new color names produces rapid increase in gray matter in the intact adult human cortex , 2011, Proceedings of the National Academy of Sciences.

[62]  S. Zeki,et al.  The neural basis of romantic love , 2000, Neuroreport.

[63]  Lutz Jäncke,et al.  The neuroanatomy of grapheme–color synesthesia , 2009, The European journal of neuroscience.

[64]  G. McCarthy,et al.  Dissociable prefrontal brain systems for attention and emotion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[65]  E. T. Bullmore,et al.  Functional magnetic resonance imaging of synesthesia: activation of V4/V8 by spoken words , 2002, Nature Neuroscience.