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White matter correlates of hemi-face dominance in happy and sad expression

Abstract

The neural underpinnings of human emotional expression are thought to be unevenly distributed among the two brain hemispheres. However, little is known on the anatomy supporting this claim, particularly in the cerebral white matter. Here, we explored the relationship between hemi-face dominance in emotional expression and cerebral white matter asymmetries in 33 healthy participants. Measures of emotional expression were derived from pictures of the participant’s faces in a ‘happy smiling’ and a ‘sad frowning’ conditions. Chimeric faces were constructed by mirroring right and left hemi-faces, as done in previous studies, resulting in a left mirrored and right mirrored chimeric face per picture. To gain measures of hemi-face dominance per participant, a jury of 20 additional participants rated which chimeric face shows the higher intensity of emotional expressivity, by marking a 155 mm line between the two versions. Measures of the asymmetry of the uncinate, the cingulum and the three branches of superior longitudinal fasciculi were derived from diffusion-weighted imaging tractography dissections. Group effect analyses indicated that the degree of asymmetry in emotional expression was not as prominent as reported in the literature and showed a large inter-individual variability. The degree of asymmetry in emotional expression was, however, significantly associated with the asymmetries in connective properties of the fronto-temporal and fronto-parietal tracts, specifically the uncinate fasciculus and the first branch of the superior longitudinal fasciculus. Therefore, this result raises novel hypotheses on the relationship of specific white matter tracts and emotional expression, especially their role in mood disorders.

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References

  1. Agosta F, Scola E, Canu E, Marcone A, Magnani G, Sarro L et al (2012) White matter damage in frontotemporal lobar degeneration spectrum. Cereb Cortex 22(12):2705–2714

  2. Alexander D (2005) Multiple-fiber reconstruction algorithms for diffusion MRI. Ann N Y Acad Sci 1064(1):113–133

  3. Alves PN, Foulon C, Karolis V, Bzdok D, Margulies DS, Volle E, Thiebaut de Schotten M (2019) An improved neuroanatomical model of the default-mode network reconciles previous neuroimaging and neuropathological findings. Commun Biol. https://doi.org/10.1038/s42003-019-0611-3

  4. Anderson A (2005) Measurement of fiber orientation distributions using high angular resolution diffusion imaging. Magn Reson Med 54(5):1194–1206

  5. Andersson J, Skare S, Ashburner J (2003) How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging. NeuroImage 20(2):870–888

  6. Babinski J (1914) Contribution of cerebral hemispheric organization in the study of mental troubles. Rev Neurol 27:845–848

  7. Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66(1):259–267

  8. Becker S, Horstmann G, Remington R (2011) Perceptual grouping, not emotion, accounts for search asymmetries with schematic faces. J Exp Psychol: Hum Percept Perform 37(6):1739–1757

  9. Berenbaum H, Rotter A (1992) The relationship between spontaneous facial expressions of emotion and voluntary control of facial muscles. J Nonverbal Behav 16(3):179–190

  10. Borod JC (1993) Cerebral mechanisms underlying facial, prosodic, and lexical emotional expression: a review of neuropsychological studies and methodological issues. Neuropsychology 7(4):445–463

  11. Borod JC, Haywood CS, Koff E (1997) Neuropsychological aspects of facial asymmetry during emotional expression: a review of the normal adult literature. Neuropsychol Rev 7(1):41–60

  12. Bradshaw JL, Lesley JR (1993) The evolution of lateral asymmetries, language, tool use, and intellect. Academic Press, San Diego

  13. Breiter H, Etcoff N, Whalen P, Kennedy W, Rauch S, Buckner R, Strauss M, Hyman S, Rosen B (1996) Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17(5):875–887

  14. Broca P (1861) Remarques sur le siège de la faculté du langage articulé, suivies d’une observation d’aphémie (perte de la parole). Bulletins de la Société d’anatomie (Paris), 2e serie 6:330–357

  15. Catani M, Flavio D, Michel TS (2013) A revised limbic system model for memory, emotion and behaviour. Neurosci Biobehav Rev 37(8):1724–1737

  16. Chechlacz M, Gillebert C, Vangkilde S, Petersen A, Humphreys G (2015) Structural variability within frontoparietal networks and individual differences in attentional functions: an approach using the theory of visual attention. J Neurosci 35(30):10647–10658

  17. Coad B, Postans M, Hodgetts C, Muhlert N, Graham K, Lawrence A (2017) Structural connections support emotional connections: uncinate Fasciculus microstructure is related to the ability to decode facial emotion expressions. Neuropsychologia. https://doi.org/10.1016/j.neuropsychologia.2017.11.006

  18. Craig AD (2005) Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 9(12):566–571

  19. Craig MC et al (2009) Altered connections on the road to psychopathy. Mol Psychiatry 14(10):946–953

  20. Dell'Acqua F, Scifo P, Rizzo G, Catani M, Simmons A, Scotti G, Fazio F (2010) A modified damped Richardson–Lucy algorithm to reduce isotropic background effects in spherical deconvolution. NeuroImage 49(2):1446–1458

  21. Dell'Acqua F, Simmons A, Williams S, Catani M (2012) Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true-tract specific index to characterize white matter diffusion. Hum Brain Mapp 34(10):2464–2483

  22. Demaree HA, Everhart DE, Youngstrom EA, Harrison DW (2005) Brain lateralization of emotional processing: historical roots and a future incorporating “dominance”. Behav Cogn Neurosci Rev 4(1):3–20

  23. Ekman P (1980) Asymmetry in facial expression. Science 209(4458):833–834

  24. Fernández-Carriba S, Loeches Á, Morcillo A, Hopkins WD (2002) Asymmetry in facial expression of emotions by chimpanzees. Neuropsychologia 40(9):1523–1533

  25. Gainotti G (2019) The role of the right hemisphere in emotional and behavioral disorders of patients with frontotemporal lobar degeneration: an updated review. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2019.00055

  26. Hau J, Sarubbo S, Houde JC, Corsini F, Girard G, Deledalle C et al (2017) Revisiting the human uncinate fasciculus, its subcomponents and asymmetries with stem-based tractography and microdissection validation. Brain Struct Funct 222(4):1645–1662

  27. Hauser M (1993) Right hemisphere dominance for the production of facial expression in monkeys. Science 261(5120):475–477

  28. Hellige JB (2001) Hemispheric asymmetry, 1st edn. Harvard University Press, Cambridge

  29. Highley JR (2002) Asymmetry of the uncinate fasciculus: a post-mortem study of normal subjects and patients with schizophrenia. Cereb Cortex 12(11):1218–1224

  30. Hodsoll S, Viding E, Lavie N (2011) Attentional capture by irrelevant emotional distractor faces. Emotion 11(2):346–353. https://doi.org/10.1037/a0022771

  31. Jenkins L, Barba A, Campbell M, Lamar M, Shankman S, Leow A, Ajilore O, Langenecker S (2016) Shared white matter alterations across emotional disorders: a voxel-based meta-analysis of fractional anisotropy. NeuroImage Clin 12:1022–1034

  32. Jewell G, McCourt M (2000) Pseudoneglect: a review and meta-analysis of performance factors in line bisection tasks. Neuropsychologia 38(1):93–110

  33. Karolis VR, Corbetta M, Thiebaut de Schotten M (2019) The architecture of functional lateralisation and its relationship to callosal connectivity in the human brain. Nat Commun 10(1):1417

  34. Kern M, Bert S, Glanz O, Schulze-Bonhage A, Ball T (2019) Human motor cortex relies on sparse and action-specific activation during laughing, smiling and speech production. Commun Biol. https://doi.org/10.1038/s42003-019-0404-8

  35. MacLean PD (1952) Some psychiatric implications of physiological studies on frontotemporal portion of limbic system (visceral brain). Electroencephalogr Clin Neurophysiol 4:407–418

  36. Matsuo K, Mizuno T, Yamada K, Akazawa K, Kasai T, Kondo M et al (2008) Cerebral white matter damage in frontotemporal dementia assessed by diffusion tensor tractography. Neuroradiology 50(7):605–611

  37. Mesulam M (2000) Behavioural neuroanatomy: large-scale networks, association cortex, frontal syndromes, the limbic system, and the hemispheric specializations. In: Mesulam M (ed) Principles of behavioural and cognitive neurology, pp 1–120

  38. Mills CK (1912) The cerebral mechanisms of emotional expression. Trans Coll Phys Phila 34:381–390

  39. Morris RD, Hopkins WD (1993) Perception of human chimeric faces by chimpanzees: evidence for a right hemisphere advantage. Brain Cogn 21(1):111–122

  40. Ocklenburg S, Friedrich P, Güntürkün O, Genc E (2016) Intrahemispheric white matter asymmetries: the missing link between brain structure and functional lateralization? Rev Neurosci 27(5):465–480

  41. Parlatini V, Radua J, Dell’Acqua F, Leslie A, Simmons A, Murphy D, Catani M, Thiebaut de Schotten M (2017) Functional segregation and integration within fronto-parietal networks. NeuroImage 146:367–375

  42. Phelps EA (2006) Emotion and cognition: insights from studies of the human amygdala. Annu Rev Psychol 57(1):27–53

  43. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48(2):175–187

  44. Piguet O, Hornberger M, Mioshi E, Hodges JR (2011) Behavioural-variant frontotemporal dementia: diagnosis, clinical staging, and management. Lancet Neurol 10(2):162–172

  45. Raichle M, Snyder A (2007) A default mode of brain function: a brief history of an evolving idea. NeuroImage 37(4):1083–1090

  46. Raichle M, MacLeod A, Snyder A, Powers W, Gusnard D, Shulman G (2001) A default mode of brain function. Proc Natl Acad Sci 98(2):676–682

  47. Rinn WB (1984) The neuropsychology of facial expression: a review of the neurological and psychological mechanisms for producing facial expression. Psychol Bull 95:52–77

  48. Rojkova K, Volle E, Urbanski M, Dell’Acqua F, Thiebaut de Schotten M (2016) Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct 221(3):1751–1766. https://doi.org/10.1007/s00429-015-1001-3

  49. Ross E, Pulusu V (2013) Posed versus spontaneous facial expressions are modulated by opposite cerebral hemispheres. Cortex 49(5):1280–1291. https://doi.org/10.1016/j.cortex.2012.05.002

  50. Sackeim H, Gur R, Saucy M (1978) Emotions are expressed more intensely on the left side of the face. Science 202(4366):434–436

  51. Satpute AB, Lindquist KA (2019) The default mode network's role in discrete emotion. Trends Cogn Sci 23(10):851–864

  52. Schmahmann J, Pandya D, Wang R, Dai G, D'Arceuil H, de Crespigny A, Wedeen V (2007) Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130(3):630–653

  53. Seghier ML (2008) Laterality index in functional MRI: methodological issues. Magn Reson Imaging 26(5):594–601

  54. Silberman EK, Weingartner H (1986) Hemispheric lateralization of functions related to emotion. Brain Cogn 5(3):322–353

  55. Skinner M, Mullen B (1991) Facial asymmetry in emotional expression: a meta-analysis of research. Br J Soc Psychol 30(2):113–124. https://doi.org/10.1111/j.2044-8309.1991.tb00929.x

  56. Smith S, Jenkinson M, Woolrich M, Beckmann C, Behrens T, Johansen-Berg H, Bannister P, De Luca M, Drobnjak I, Flitney D, Niazy R, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady J, Matthews P (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23:S208–S219

  57. Sperry RW (1974) Lateral specialization in the surgically separated hemispheres, Ch. I. In: Schmitt F, Worden F (eds) Neurosciences third study program, vol 3. MIT Press, Cambridge, pp 5–19

  58. Thiebaut de Schotten M, Ffytche D, Bizzi A, Dell'Acqua F, Allin M, Walshe M, Murray R, Williams S, Murphy D, Catani M (2011a) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. NeuroImage 54(1):49–59

  59. Thiebaut de Schotten M, Dell'Acqua F, Forkel S, Simmons A, Vergani F, Murphy D, Catani M (2011b) A lateralized brain network for visuospatial attention. Nat Neurosci 14(10):1245–1246

  60. Thiebaut de Schotten M, Shallice T (2017) Identical, similar or different? Is a single brain model sufficient? Cortex 86:172–175

  61. Thiebaut de Schotten, M., Friedrich, P., & Forkel, S. J. (2019). One size fits all does not apply to brain lateralisation Comment on “Phenotypes in hemispheric functional segregation? Perspectives and challenges” by Guy Vingerhoets. Physics of life reviews.

  62. Tournier J, Calamante F, Gadian D, Connelly A (2004) Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. NeuroImage 23(3):1176–1185

  63. Vingerhoets G (2019) Toward a multidimensional description of individual variation in hemispheric functional segregation: Reply to comments on "Phenotypes in hemispheric functional segregation? Perspectives and challenges. Phys Life Rev 30:41–46. https://doi.org/10.1016/j.plrev.2019.10.011

  64. Whitwell JL, Avula R, Senjem ML, Kantarci K, Weigand SD, Samikoglu A et al (2010) Gray and white matter water diffusion in the syndromic variants of frontotemporal dementia. Neurology 74(16):1279–1287

  65. Yakovlev PJ (1948) Motility, behavior and the brain; stereodynamic organization and neural coordinates of behavior. J Nerv Ment Dis 107:313–335

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Acknowledgements

We thank ERASMUS for supporting SI. This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (Grant agreement No. 818521). The research leading to these results also received funding from the “Agence Nationale de la Recherche” [Grants number ANR-13-JSV4-0001-01] and from the Fondation pour la Recherche Médicale (FRM). Additional financial support comes from the program “Investissements d’avenir” ANR-10-IAIHU-06 and ANR-11-INBS-0006.

Funding

Funding from ERC (Grant agreement No. 818521) and “Agence Nationale de la Recherche” [Grants numbers ANR-13- JSV4-0001-01, ANR-10-IAIHU-06 and ANR-11-INBS-0006].

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Correspondence to Stefano Ioannucci or Michel Thiebaut de Schotten.

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Data collection from human participants was approved by the Comité de Protection des Personnes "CPP Ile de France V".

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Ioannucci, S., George, N., Friedrich, P. et al. White matter correlates of hemi-face dominance in happy and sad expression. Brain Struct Funct (2020). https://doi.org/10.1007/s00429-020-02040-7

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Keywords

  • Asymmetry
  • Emotion expression
  • Lateralization
  • White matter
  • Neuroanatomy