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Brain Topography

, Volume 30, Issue 6, pp 774–784 | Cite as

Putamen Volume is Negatively Correlated with the Ability to Recognize Fearful Facial Expressions

  • Shota Uono
  • Wataru Sato
  • Takanori Kochiyama
  • Yasutaka Kubota
  • Reiko Sawada
  • Sayaka Yoshimura
  • Motomi Toichi
Original Paper

Abstract

Findings of previous functional magnetic resonance imaging (MRI) and neuropsychological studies have suggested that specific aspects of the basal ganglia, particularly the putamen, are involved in the recognition of emotional facial expressions. However, it remains unknown whether variations in putamen structure reflect individual differences in the ability to recognize facial expressions. Thus, the present study assessed the putamen volumes and shapes of 50 healthy Japanese adults using structural MRI scans and evaluated the ability of participants to recognize facial expressions associated with six basic emotions: anger, disgust, fear, happiness, sadness, and surprise. The volume of the bilateral putamen was negatively associated with the recognition of fearful faces, and the local shapes of both the anterior and posterior subregions of the bilateral putamen, which are thought to support cognitive/affective and motor processing, respectively, exhibited similar negative relationships with the recognition of fearful expressions. These results suggest that individual differences in putamen structure can predict the ability to recognize fearful facial expressions in others. Additionally, these findings indicate that cognitive/affective and motor processing underlie this process.

Keywords

Basal ganglia Emotion recognition Fearful face Structural magnetic resonance imaging Putamen 

Notes

Acknowledgements

We thank the ATR Brain Activity Imaging Center for their support in acquiring the data, Kazusa Minemoto, Akemi Inoue, and Emi Yokoyama for their technical support, and our anonymous reviewers for their helpful advice. Our study was supported by the JSPS Funding Program for Next Generation World-Leading Researchers (LZ008). The funding sources had no involvement in the study design; in the collection, analysis and interpretation of the data; in the writing of the report; or in the decision to submit the article for publication. The authors declare no competing interests.

Supplementary material

10548_2017_578_MOESM1_ESM.doc (301 kb)
Supplementary material 1 (DOC 301 KB)

References

  1. Adolphs R, Gosselin F, Buchanan TW, Tranel D, Schyns P, Damasio AR (2005) A mechanism for impaired fear recognition agfter amygdala damage. Nature 433:68–72. doi: 10.1038/nature03086 CrossRefPubMedGoogle Scholar
  2. Arsalidou M, Morris D, Taylor MJ (2011) Converging evidence for the advantage of dynamic facial expressions. Brain Topogr 24:149–163. doi: 10.1007/s10548-011-0171-4 CrossRefPubMedGoogle Scholar
  3. Arsalidou M, Duerden EG, Taylor MJ (2013) The centre of the brain: Topographical model of motor, cognitive, affective, and somatosensory functions of the basal ganglia. Hum Brain Map 34:3031–3054. doi: 10.1002/hbm.22124 CrossRefGoogle Scholar
  4. Baker RS, Anderson AH, Morecraft RJ, Smith CD (2003) A functional magnetic resonance imaging study in patients with benign essential blepharospasm. J Neuro-Ophthalmol 23:11–15CrossRefGoogle Scholar
  5. Baron-Cohen S, Ring HA, Wheelwright S, Bullmore E, Brammer MJ, Simmons A, Williams SCR (1999) Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci 11:1891–1898CrossRefPubMedGoogle Scholar
  6. Black KJ, Ongür D, Perlmutter JS (1998) Putamen volume in idiopathic focal dystonia. Neurology 51:819–824CrossRefPubMedGoogle Scholar
  7. Bora E, Fornito A, Pantelis C, Yucel M (2012) Gray matter abnormalities in major depressive disorder: A meta-analysis of voxel based morphometry studies. J Affect Disord 138:9–18. doi: 10.1016/j.jad.2011.03.049 CrossRefPubMedGoogle Scholar
  8. Calder AJ, Keane J, Manes F, Antoun N, Young AW (2000) Impaired recognition and experience of disgust following brain injury. Nat Neurosci 3:1077–1078CrossRefPubMedGoogle Scholar
  9. Calder AJ, Keane J, Lawrence AD, Manes F (2004) Impaired recognition of anger following damage to the ventral striatum. Brain 127:1958–1969CrossRefPubMedGoogle Scholar
  10. Circelli K, Clark US, Cronin-Golomb A (2013) Visual scanning patterns and executive function in relation to facial emotion recognition in aging. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 20:148–173. doi: 10.1080/13825585.2012.675427 CrossRefPubMedGoogle Scholar
  11. Dalili MN, Penton-Volak IS, Harmer CJ, Munafò MR (2015) Meta-analysis of emotion recognition deficits in major depressive disorder. Psychol Med 45:1135–1144. doi: 10.1017/S0033291714002591 CrossRefPubMedGoogle Scholar
  12. Dawel A, O’Kearney R, McKone E, Palermo R (2012) Not just fear and sadness: meta-analytic evidence of pervasive emotion recognition deficits for facial and vocal expressions in psychopathy. Neurosci Biobehav Rev 36:2288–2304. doi: 10.1016/j.neubiorev.2012.08.006 CrossRefPubMedGoogle Scholar
  13. DeLong MR, Wichmann T (2007) Circuits and circuit disorders of the basal ganglia. Neurol Rev 64:200–224Google Scholar
  14. Draganski B, Kherif F, Kloppel S, Cook PA, Alexander DC, Parker GJ, Deichmann R, Ashburner J, Frackowiak RSJ (2008) Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J Neurosci 28:7143–7152. doi: 10.1523/JNEUROSCI.1486-08.2008 CrossRefPubMedGoogle Scholar
  15. Ekman P, Friesen WV (1976) Pictures of facial affect. Consulting Psychologists Press, Palo AltoGoogle Scholar
  16. Ekman P, Friesen WV (1978) Facial action coding system: a technique for the measurement of facial movement. Consulting Psychologists Press, Palo AltoGoogle Scholar
  17. Etgen T, Muhlau M, Gaser C, Sander D (2006) Bilateral grey-matter increase in the putamen in primary blepharospasm. J Neurol Neurosurg Psychiatry 77:1017–1020CrossRefPubMedPubMedCentralGoogle Scholar
  18. Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, Benedetti F, Abbamonte M, Gasparotti R, Barale F, Perez J, McGuire P, Politi P (2009) Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 34:418–432PubMedPubMedCentralGoogle Scholar
  19. George M, Ketter TA, Parekh PI, Horwitz B, Herscovitch P, Post RM (1995) Brain activity during transient sadness and happiness in healthy women. Am J Psychiatry 152:341–351CrossRefPubMedGoogle Scholar
  20. Gerardin E, Lehéricy S, Pochon JB, Tézenas du Montcel S, Mangin JF, Poupon F, Agid Y, Le Bihan D, Marsault C (2003) Foot, hand, face and eye representation in the human striatum. Cereb Cortex 13:162–169CrossRefPubMedGoogle Scholar
  21. Grahn JA, Parkinson JA, Owen AM (2008) The cognitive functions of the caudate nucleus. Prog Neurobiol 86:141–155. doi: 10.1016/j.pneurobio.2008.09.004 CrossRefPubMedGoogle Scholar
  22. Gray HM, Tickle-Degnen L (2010) A meta-analysis of performance on emotion recognition tasks in Parkinson’s disease. Neuropsychology 24:176–191. doi: 10.1037/a0018104 CrossRefPubMedGoogle Scholar
  23. Henley SM, Novak MJ, Frost C, King J, Tabriz SJ, Warren JD (2012) Emotion recognition in Huntington’s disease: a systematic review. Neurosci Biobehav Rev 36:237–253. doi: 10.1016/j.neubiorev.2011.06.002 CrossRefPubMedGoogle Scholar
  24. Hidano N, Fukuhara M, Iwawaki M, Soga S, Spielberger CD (2000) Manual for the state-trait anxiety inventory-form JYZ. Jitsumu-Kyoiku-Shuppan, TokyoGoogle Scholar
  25. Kojima M, Furukawa T (2003) The Japanese version of Beck depression inventory-II (BDI-II). Nihon-Bunka-Kagaku-Sha, TokyoGoogle Scholar
  26. Kret ME, de Gelder B (2012) A review on sex differences in processing emotional signals. Neuropsychologia 50:1211–1221. doi: 10.1016/j.neuropsychologia.2011.12.022 CrossRefPubMedGoogle Scholar
  27. Lange K, Williams LM, Young AW, Bullmore ET, Williams SCR, Gray JA, Phillips ML (2003) Task instructions modulate neural responses to fearful facial expression. Biol Psychiatry 53:226–232CrossRefPubMedGoogle Scholar
  28. Lee TM, Ng EH, Tang SW, Chan CC (2008) Effects of sad mood on facial emotion recognition in Chinese people. Psychiatry Res 159:37–43. doi: 10.1016/j.psychres.2007.04.022 CrossRefPubMedGoogle Scholar
  29. Matsumoto D, Ekman P (1988) Japanese and Caucasian facial expressions of emotion. Intercultural and Emotion Research Laboratory, Department of Psychology, San Francisco State University, San FranciscoGoogle Scholar
  30. Nemmi F, Sabatini U, Rascol O, Peran P (2015) Parkinson’s disease and local atrophy in subcortical nuclei: insight from shape analysis. Neurobiol Aging 36:424–433. doi: 10.1016/j.neurobiolaging.2014.07.010 CrossRefPubMedGoogle Scholar
  31. Niedenthal PM (2007) Embodying emotion. Science 316:1002–1005CrossRefPubMedGoogle Scholar
  32. Oberman LM, Winkielman P, Ramachandran VS (2007) Face to face: Blocking facial mimicry can selectively impair recognition of emotional expressions. Soc Neurosci 2:167–178. doi: 10.1080/17470910701391943 CrossRefPubMedGoogle Scholar
  33. Okada T, Kubota Y, Sato W, Murai T, Pellion F, Gorog F (2015) Common impairments of emotional facial expression recognition in schizophrenia across French and Japanese cultures. Front Psychol 6:1018. doi: 10.3389/fpsyg.2015.01018 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Oldfield RC (1971) The assessment and analysis of handness: the Edinburgh inventory. Neuropsychologia 9:97–113CrossRefPubMedGoogle Scholar
  35. Otsubo T, Miyaoka H, Kamijima K (2005) M.I.N.I. Mini international neuropsychiatric interview. Seiwa Shoten, TokyoGoogle Scholar
  36. Pardini DA, Raine A, Erickson K, Loeber R (2014) Lower amygdala volume in men is associated with childhood aggression, early psychopathic traits, and future violence. Biol Psychiatry 75:73–80. doi: 10.1016/j.biopsych.2013.04.003 CrossRefPubMedGoogle Scholar
  37. Patenaude B (2007) Bayesian statistical models of shape and appearance for subcortical brain segmentation. University of Oxford, OxfordGoogle Scholar
  38. Patenaude B, Smith SM, Kennedy DN, Jenkinson M (2011) A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 56:907–922. doi: 10.1016/j.neuroimage.2011.02.046 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Pauli WM, O’Reilly RC, Yarkoni T, Wagerb TD (2016) Regional specialization within the human striatum for diverse psychological functions. Proc Natl Acad Sci USA 113:1907–1912. doi: 10.1073/pnas.1507610113 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Phillips ML, Young AW, Scott SK, Calder AJ, Andrew C, Giampietro V, Williams SC, Bullmore ET, Brammer M, Gray JA (1998) Neural responses to facial and vocal expressions of fear and disgust. Proc R Soc Lond B 265:1809–1817CrossRefGoogle Scholar
  41. Pitcher TL, Melzer TR, Macaskill MR, Graham CF, Livingston L, Keenan RJ, Watts R, Dalrymple-Alford JC, Anderson TJ (2012) Reduced striatal volumes in Parkinson’s disease: A magnetic resonance imaging study. Transl Neurodegener 1:17. doi: 10.1186/2047-9158-1-17.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Richards A, French CC, Calder AJ, Webb B, Fox R, Young AW (2002) Anxiety-related bias in the classification of emotionally ambiguous facial expressions. Emotion 2:273–287CrossRefPubMedGoogle Scholar
  43. Ruigrok AN, Salimi-Khorshidi G, Lai MC, Baron-Cohen S, Lombardo MV, Tait RJ, Suckling J (2014) A meta-analysis of sex differences in human brain structure. Neurosci Biobehav Rev 39:34–50. doi: 10.1016/j.neubiorev.2013.12.004 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Sato W, Kubota Y, Okada T, Murai T, Yoshikawa S, Sungoku A (2002) Seeing happy emotion in fearful and angry faces: qualitative analysis of facial expression recognition in a bilateral amygdala-damaged patient. Cortex 38:727–742CrossRefPubMedGoogle Scholar
  45. Sato W, Fujimura T, Kochiyama T, Suzuki N (2013a) Relationships among facial mimicry, emotional experience, and emotion recognition. PLoS ONE 8:e57889. doi: 10.1371/journal.pone.0057889 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Sato W, Kochiyama T, Uono S, Matsuda K, Usui K, Inoue Y, Toichi M (2013b) Rapid and multiple-stage activation of the human amygdala for processing facial signals. Commun Integr Biol 6:e24562. doi: 10.4161/cib.24562 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Sato W, Kubota Y, Kochiyama T, Uono S, Yoshimura S, Sawada R, Sakihama M, Toichi M (2014) Increased putamen volume in adults with autism spectrum disorder. Front Hum Neurosci 8:957. doi: 10.3389/fnhum.2014.00957 PubMedPubMedCentralGoogle Scholar
  48. Sato W, Kochiyama T, Uono S, Yoshikawa S, Toichi M (2017) Direction of amygdala-neocortex interaction during dynamic facial expression processing. Cereb Cortex 27:1878–1890. doi: 10.1093/cercor/bhw036 PubMedGoogle Scholar
  49. Schmidt KE, Linen DEJ, Goebel R, Zanella FE, Lanfermann H, Zubcov A (2003) Striatal activation during blepharospasm revealed by fMRI. Neurology 60:1738–1743CrossRefPubMedGoogle Scholar
  50. Shang J, Fu Y, Ren Z, Zhang T, Du M, Gong Q, Lui S, Zhang W (2014) The common traits of the ACC and PFC in anxiety disorders in the DSM-5: Meta-analysis of voxel-based morphometry studies. PLoS ONE 9:e93432. doi: 10.1371/journal.pone.0093432 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Smith SM, Nichols TE (2009) Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44:8398. doi: 10.1016/j.neuroimage.2008.03.061 Google Scholar
  52. Surcinelli P, Codispoti M, Montebarocci O, Rossi N, Baldaro B (2006) Facial emotion recognition in trait anxiety. J Anxiety Disord 20:110–117CrossRefPubMedGoogle Scholar
  53. Uono S, Sato W, Toichi M (2011) The specific impairment of fearful expression recognition and its atypical development in pervasive developmental disorder. Soc Neurosci 6:452–463. doi: 10.1080/17470919.2011.605593 CrossRefPubMedGoogle Scholar
  54. Uono S, Sato W, Toichi M (2013) Common and unique impairments in facial-expression recognition in pervasive developmental disorder-not otherwise specified and Asperger’s disorder. Res Autism Spect Disord 7:361–368. doi: 10.1016/j.rasd.2012.10.007 CrossRefGoogle Scholar
  55. Uono S, Sato W, Toichi M (2014) Reduced representational momentum for subtle dynamic facial expressions in individuals with autism spectrum disorders. Res Autism Spectr Disord 8:1090–1099. doi: 10.1016/j.rasd.2014.05.018 CrossRefGoogle Scholar
  56. van den Heuvel OA, Veltman DJ, Groenewegen HJ, Cath DC, van Balkom AJ, van Hartskamp J, Barkhof F, van Dyck R (2005) Frontal-striatal dysfunction during planning in obsessive-compulsive disorder. Arch Gen Psychiatry 62:301–309CrossRefPubMedGoogle Scholar
  57. Verghese J, Milling C, Rosenbaum DM (1999) Ptosis, blepharospasm, and apraxia of eyelid opening secondary to putaminal hemorrhage. Neurology 53:652CrossRefPubMedGoogle Scholar
  58. Walker FO (2007) Huntington’s disease. Lancet 369:218–228CrossRefPubMedGoogle Scholar
  59. Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE (2014) Permutation inference for the general linear model. Neuroimage 92:381–397. doi: 10.1016/j.neuroimage.2014.01.060 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Yang Y, Narr KL, Baker LA, Joshi SH, Jahanshad N, Raine A, Thompson PM (2015) Frontal and striatal alterations associated with psychopathic traits in adolescents. Psychiatry Res 231:333–340. doi: 10.1016/j.pscychresns.2015.01.017 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Yoshimura S, Sato W, Uono S, Toichi M (2015) Impaired overt facial mimicry in response to dynamic facial expressions in high-functioning autism spectrum disorders. J Autism Dev Disord 45:1318–1328. doi: 10.1007/s10803-014-2291-7 CrossRefPubMedGoogle Scholar
  62. Zhao K, Yan WJ, Chen YH, Zuo XN, Fu X (2013) Amygdala volume predicts inter-individual differences in fearful face recognition. PLoS ONE 8:e74096. doi: 10.1371/journal.pone.0074096 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Zhao K, Zhao J, Zhang M, Cui Q, Fu X (2017) Neural responses to rapid facial expressions of fear and surprise. Front Psychol 8:761. doi: 10.3389/fpsyg.2017.00761 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Shota Uono
    • 1
  • Wataru Sato
    • 1
  • Takanori Kochiyama
    • 2
  • Yasutaka Kubota
    • 3
  • Reiko Sawada
    • 1
    • 4
  • Sayaka Yoshimura
    • 1
  • Motomi Toichi
    • 4
    • 5
  1. 1.Department of Neurodevelopmental Psychiatry, Habiliration, and Rehabilitation, Graduate School of MedicineKyoto UniversityKyotoJapan
  2. 2.ATR Brain Activity Imaging CenterKyotoJapan
  3. 3.Health and Medical Services CenterShiga UniversityHikoneJapan
  4. 4.The Organization for Promoting Neurodevelopmental Disorder ResearchKyotoJapan
  5. 5.Faculty of Human Health Sciences, Graduate School of MedicineKyoto UniversityKyotoJapan

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