Cognitive, Affective, & Behavioral Neuroscience

, Volume 18, Issue 6, pp 1188–1197 | Cite as

TMS over the superior temporal sulcus affects expressivity evaluation of portraits

  • Chiara Ferrari
  • Susanna Schiavi
  • Zaira Cattaneo
Original Research


When viewing a portrait, we are often captured by its expressivity, even if the emotion depicted is not immediately identifiable. If the neural mechanisms underlying emotion processing of real faces have been largely clarified, we still know little about the neural basis of evaluation of (emotional) expressivity in portraits. In this study, we aimed at assessing—by means of transcranial magnetic stimulation (TMS)—whether the right superior temporal sulcus (STS) and the right somatosensory cortex (SC), that are important in discriminating facial emotion expressions, are also causally involved in the evaluation of expressivity of portraits. We found that interfering via TMS with activity in (the face region of) right STS significantly reduced the extent to which portraits (but not other paintings depicting human figures with faces only in the background) were perceived as expressive, without, though, affecting their liking. In turn, interfering with activity of the right SC had no impact on evaluating either expressivity or liking of either paintings’ category. Our findings suggest that evaluation of emotional cues in artworks recruit (at least partially) the same neural mechanisms involved in processing genuine biological others. Moreover, they shed light on the neural basis of liking decisions in art by art-naïve people, supporting the view that aesthetic appreciation relies on a multitude of factors beyond emotional evaluation.


STS TMS Artworks Emotion 



This work was supported by a PRIN grant (2015WXAXJF) by Italian Ministry of Education, University and Research to Z.C.

Supplementary material

13415_2018_630_MOESM1_ESM.docx (176 kb)
ESM 1 (DOCX 176 kb)


  1. Adams, R. B., Jr., & Kleck, R. E. (2005). Effects of direct and averted gaze on the perception of facially communicated emotion. Emotion, 5(1), 3–11.CrossRefPubMedGoogle Scholar
  2. Adolphs, R., Damasio, H., Tranel, D., Cooper, G., & Damasio, A. R. (2000). A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. Journal of Neuroscience, 20(7), 2683–2690.CrossRefPubMedGoogle Scholar
  3. Atkinson, A. P., & Adolphs, R. (2011). The neuropsychology of face perception: Beyond simple dissociations and functional selectivity. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 366(1571), 1726–1738.CrossRefPubMedGoogle Scholar
  4. Avenanti, A., Candidi, M., & Urgesi, C. (2013). Vicarious motor activation during action perception: Beyond correlational evidence. Frontiers in Human Neuroscience, 7, 185.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Balconi, M., & Ferrari, C. (2013a). Left DLPFC rTMS stimulation reduced the anxiety bias effect or how to restore the positive memory processing in high-anxiety subjects. Psychiatry Research, 209(3), 554–559.CrossRefPubMedGoogle Scholar
  6. Balconi, M., & Ferrari, C. (2013b). Repeated transcranial magnetic stimulation on dorsolateral prefrontal cortex improves performance in emotional memory retrieval as a function of level of anxiety and stimulus valence. Psychiatry and Clinical Neurosciences, 67(4), 210–218.CrossRefPubMedGoogle Scholar
  7. Barraclough, N. E., Xiao, D., Oram, M. W., & Perrett, D. I. (2006). The sensitivity of primate STS neurons to walking sequences and to the degree of articulation in static images. Progress in Brain Research, 154, 135–148.CrossRefPubMedGoogle Scholar
  8. Boccia, M., Barbetti, S., Piccardi, L., Guariglia, C., Ferlazzo, F., Giannini, A. M., & Zaidel, D. W. (2016). Where does brain neural activation in aesthetic responses to visual art occur? Meta-analytic evidence from neuroimaging studies. Neuroscience & Biobehavioral Reviews, 60, 65–71.CrossRefGoogle Scholar
  9. Bona, S., Cattaneo, Z., & Silvanto, J. (2015). The causal role of the occipital face area (OFA) and lateral occipital (LO) cortex in symmetry perception. Journal of Neuroscience, 35(2), 731–738.CrossRefPubMedGoogle Scholar
  10. Boyarskaya, E., Sebastian, A., Bauermann, T., Hecht, H., & Tüscher, O. (2015). The Mona Lisa effect: Neural correlates of centered and off-centered gaze. Human Brain Mapping, 36(2), 619–632.CrossRefPubMedGoogle Scholar
  11. Calvo-Merino, B., Urgesi, C., Orgs, G., Aglioti, S. M., & Haggard, P. (2010). Extrastriate body area underlies aesthetic evaluation of body stimuli. Experimental Brain Research, 204(3), 447–456.CrossRefPubMedGoogle Scholar
  12. Carducci, F., & Brusco, R. (2012). Accuracy of an individualized MR-based head model for navigated brain stimulation. Psychiatry Research: Neuroimaging, 203(1), 105–108.CrossRefPubMedGoogle Scholar
  13. Carlin, J. D., & Calder, A. J. (2013). The neural basis of eye gaze processing. Current Opinion in Neurobiology, 23(3), 450–455.CrossRefPubMedGoogle Scholar
  14. Casile, A. (2013). Mirror neurons (and beyond) in the macaque brain: An overview of 20 years of research. Neuroscience Letters, 540, 3–14.CrossRefPubMedGoogle Scholar
  15. Cattaneo, Z., Lega, C., Ferrari, C., Vecchi, T., Cela-Conde, C. J., Silvanto, J., & Nadal, M. (2015). The role of the lateral occipital cortex in aesthetic appreciation of representational and abstract paintings: A TMS study. Brain and Cognition, 95, 44–53.CrossRefPubMedGoogle Scholar
  16. Cattaneo, Z., Lega, C., Flexas, A., Nadal, M., Munar, E., & Cela-Conde, C. J. (2014a). The world can look better: Enhancing beauty experience with brain stimulation. Social Cognitive and Affective Neuroscience. 9(11), 1713–1721.CrossRefPubMedGoogle Scholar
  17. Cattaneo, Z., Lega, C., Gardelli, C., Merabet, L. B., Cela-Conde, C. J., & Nadal, M. (2014b). The role of prefrontal and parietal cortices in aesthetic appreciation of representational and abstract art: A TMS study. NeuroImage, 99, 443–450.CrossRefPubMedGoogle Scholar
  18. Cattaneo, Z., Schiavi, S., Silvanto, J., & Nadal, M. (2017). A TMS study on the contribution of visual area V5 to the perception of implied motion in art and its appreciation. Cognitive Neuroscience, 8(1), 59–68.CrossRefPubMedGoogle Scholar
  19. Cazzato, V., Mele, S., & Urgesi, C. (2014). Gender differences in the neural underpinning of perceiving and appreciating the beauty of the body. Behavioural Brain Research, 264, 188–196.CrossRefPubMedGoogle Scholar
  20. Cazzato, V., Mele, S., & Urgesi, C. (2016). Different contributions of visual and motor brain areas during liking judgments of same-and different-gender bodies. Brain Research, 1646, 98–108.CrossRefPubMedGoogle Scholar
  21. Cela-Conde, C. J., Ayala, F. J., Munar, E., Maestú, F., Nadal, M., Capó, M. A., … Marty, G. (2009). Sex-related similarities and differences in the neural correlates of beauty. Proceedings of the National Academy of Sciences, 106(10), 3847–3852.CrossRefGoogle Scholar
  22. Cela-Conde, C. J., Marty, G., Maestú, F., Ortiz, T., Munar, E., Fernández, A., … Quesney, F. (2004). Activation of the prefrontal cortex in the human visual aesthetic perception. Proceedings of the National Academy of Sciences of the United States of America, 101(16), 6321–6325.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Chatterjee, A., Thomas, A., Smith, S. E., & Aguirre, G. K. (2009). The neural response to facial attractiveness. Neuropsychology, 23(2), 135–143.CrossRefPubMedGoogle Scholar
  24. Chatterjee, A., & Vartanian, O. (2014). Neuroaesthetics. Trends in Cognitive Sciences, 18(7), 370–375.CrossRefPubMedGoogle Scholar
  25. Chatterjee, A., & Vartanian, O. (2016). Neuroscience of aesthetics. Annals of the New York Academy of Sciences, 1369(1), 172–194.CrossRefPubMedGoogle Scholar
  26. Cohen Kadosh, K. C., Henson, R. N., Kadosh, R. C., Johnson, M. H., & Dick, F. (2010). Task-dependent activation of face-sensitive cortex: An fMRI adaptation study. Journal of Cognitive Neuroscience, 22(5), 903–917.CrossRefPubMedGoogle Scholar
  27. Cupchik, G. C., Vartanian, O., Crawley, A., & Mikulis, D. J. (2009). Viewing artworks: Contributions of cognitive control and perceptual facilitation to aesthetic experience. Brain and Cognition, 70(1), 84–91.CrossRefPubMedGoogle Scholar
  28. Dasgupta, S., Tyler, S. C., Wicks, J., Srinivasan, R., & Grossman, E. D. (2017). Network connectivity of the right STS in three social perception localizers. Journal of Cognitive Neuroscience, 29(2), 221–234.CrossRefPubMedGoogle Scholar
  29. de Gelder, B., Watson, R., Zhan, M., Diano, M., Tamietto, M., & Vaessen, M. (2017). Gender-specific brain activation during visual art perception. BioRxiv, 104166. doi:
  30. Devlin, J. T., & Watkins, K. E. (2007). Stimulating language: insights from TMS. Brain, 130, 610–622.CrossRefPubMedGoogle Scholar
  31. Di Dio, C., Canessa, N., Cappa, S. F., & Rizzolatti, G. (2011). Specificity of aesthetic experience for artworks: An fMRI study. Frontiers in Human Neuroscience, 5, 139.PubMedPubMedCentralGoogle Scholar
  32. Engell, A. D., & Haxby, J. V. (2007). Facial expression and gaze-direction in human superior temporal sulcus. Neuropsychologia, 45(14), 3234–3241.CrossRefPubMedGoogle Scholar
  33. Ferrari, C., Lega, C., Vernice, M., Tamietto, M., Mende-Siedlecki, P., Vecchi, T., … Cattaneo, Z. (2016a). The dorsomedial prefrontal cortex plays a causal role in integrating social impressions from faces and verbal descriptions. Cerebral Cortex, 26, 156–165.CrossRefPubMedGoogle Scholar
  34. Ferrari, C., Vecchi, T., Todorov, A., & Cattaneo, Z. (2016b). Interfering with activity in the dorsomedial prefrontal cortex via TMS affects social impressions updating. Cognitive, Affective, & Behavioral Neuroscience, 16(4), 626–634.CrossRefGoogle Scholar
  35. Fox, C. J., Moon, S. Y., Iaria, G., & Barton, J. J. (2009). The correlates of subjective perception of identity and expression in the face network: An fMRI adaptation study. NeuroImage, 44(2), 569–580.CrossRefPubMedGoogle Scholar
  36. Gerger, G., Leder, H., & Kremer, A. (2014). Context effects on emotional and aesthetic evaluations of artworks and IAPS pictures. Acta Psychologica, 151, 174–183.CrossRefPubMedGoogle Scholar
  37. Gernot, G., Pelowski, M., & Leder, H. (2018). Empathy, Einfühlung, and aesthetic experience: The effect of emotion contagion on appreciation of representational and abstract art using fEMG and SCR. Cognitive Processing, 19(2), 147–165.CrossRefPubMedGoogle Scholar
  38. Graham, D., Pallett, P. M., Meng, M., & Leder, H. (2014). Representation and aesthetics of the human face in portraiture. Art & Perception, 2(1/2), 75–98.CrossRefGoogle Scholar
  39. Graham, D., Stockinger, S., & Leder, H. (2013). An island of stability: art images and natural scenes—but not natural faces—show consistent aesthetic response in Alzheimer’s-related dementia. Frontiers in Psychology, 4, 107.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Grill-Spector, K. (2003). The neural basis of object perception. Current Opinion in Neurobiology, 13(2), 159–166.CrossRefPubMedGoogle Scholar
  41. Grossman, E. D., Battelli, L., & Pascual-Leone, A. (2005). Repetitive TMS over posterior STS disrupts perception of biological motion. Vision Research, 45(22), 2847–2853.CrossRefPubMedGoogle Scholar
  42. Hayn-Leichsenring, G. U., Kloth, N., Schweinberger, S. R., & Redies, C. (2013). Adaptation effects to attractiveness of face photographs and art portraits are domain-specific. I Perception, 4(5), 303–316.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Iacoboni, M., Koski, L. M., Brass, M., Bekkering, H., Woods, R. P., Dubeau, M. C., … Rizzolatti, G. (2001). Reafferent copies of imitated actions in the right superior temporal cortex. Proceedings of the National Academy of Sciences, 98(24), 13995–13999.CrossRefGoogle Scholar
  44. Jokisch, D., Daum, I., Suchan, B., & Troje, N. F. (2005). Structural encoding and recognition of biological motion: Evidence from event-related potentials and source analysis. Behavioural Brain Research, 157(2), 195–204.CrossRefPubMedGoogle Scholar
  45. Kesner, L., & Horáček, J. (2017). Empathy-related responses to depicted people in art works. Frontiers in Psychology, 8.Google Scholar
  46. Kirsch, L. P., Urgesi, C., & Cross, E. S. (2016). Shaping and reshaping the aesthetic brain: Emerging perspectives on the neurobiology of embodied aesthetics. Neuroscience & Biobehavioral Reviews, 62, 56–68.CrossRefGoogle Scholar
  47. Korb, S., Malsert, J., Rochas, V., Rihs, T. A., Rieger, S. W., Schwab, S., … Grandjean, D. (2015). Gender differences in the neural network of facial mimicry of smiles—An rTMS study. Cortex, 70, 101–114.CrossRefPubMedGoogle Scholar
  48. Lacey, S., Hagtvedt, H., Patrick, V. M., Anderson, A., Stilla, R., Deshpande, G., … Sathian, K. (2011). Art for reward’s sake: Visual art recruits the ventral striatum. NeuroImage, 55(1), 420–433.CrossRefPubMedGoogle Scholar
  49. Leder, H., Gerger, G., Dressler, S. G., & Schabmann, A. (2012). How art is appreciated. Psychology of Aesthetics, Creativity, and the Arts, 6(1), 2.CrossRefGoogle Scholar
  50. Lutz, A., Nassehi, A., Bao, Y., Pöppel, E., Sztrókay, A., Reiser, M., … Gutyrchik, E. (2013). Neurocognitive processing of body representations in artistic and photographic images. NeuroImage, 66, 288–292.CrossRefPubMedGoogle Scholar
  51. Makris, S., & Urgesi, C. (2014). Neural underpinnings of superior action prediction abilities in soccer players. Social Cognitive and Affective Neuroscience, 10(3), 342–351.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Marković, S. (2010). Aesthetic experience and the emotional content of paintings. Psihologija, 43(1), 47–64.CrossRefGoogle Scholar
  53. Marković, S. (2012). Components of aesthetic experience: aesthetic fascination, aesthetic appraisal, and aesthetic emotion. i-Perception, 3(1), 1–17.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Massaro, D., Savazzi, F., Di Dio, C., Freedberg, D., Gallese, V., Gilli, G., & Marchetti, A. (2012). When art moves the eyes: A behavioral and eye-tracking study. PLOS ONE, 7(5), e37285.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Mattavelli, G., Cattaneo, Z., & Papagno, C. (2011). Transcranial magnetic stimulation of medial prefrontal cortex modulates face expressions processing in a priming task. Neuropsychologia, 49(5), 992–998.CrossRefPubMedGoogle Scholar
  56. Milders, M., Hietanen, J. K., Leppänen, J. M., & Braun, M. (2011). Detection of emotional faces is modulated by the direction of eye gaze. Emotion, 11(6), 1456.CrossRefPubMedGoogle Scholar
  57. Molenberghs, P., Brander, C., Mattingley, J. B., & Cunnington, R. (2010). The role of the superior temporal sulcus and the mirror neuron system in imitation. Human Brain Mapping, 31(9), 1316–1326.CrossRefPubMedGoogle Scholar
  58. Narumoto, J., Okada, T., Sadato, N., Fukui, K., & Yonekura, Y. (2001). Attention to emotion modulates fMRI activity in human right superior temporal sulcus. Cognitive Brain Research, 12(2), 225–231.CrossRefPubMedGoogle Scholar
  59. Paracampo, R., Pirruccio, M., Costa, M., Borgomaneri, S., & Avenanti, A. (2018). Visual, sensorimotor and cognitive routes to understanding others’ enjoyment: An individual differences rTMS approach to empathic accuracy. Neuropsychologia, 116(Pt. A), 86–98. doi: CrossRefPubMedGoogle Scholar
  60. Paracampo, R., Tidoni, E., Borgomaneri, S., di Pellegrino, G., & Avenanti, A. (2017). Sensorimotor network crucial for inferring amusement from smiles. Cerebral Cortex, 27(11), 5116–5129.PubMedGoogle Scholar
  61. Pearce, M. T., Zaidel, D. W., Vartanian, O., Skov, M., Leder, H., Chatterjee, A., & Nadal, M. (2016). Neuroaesthetics: The cognitive neuroscience of aesthetic experience. Perspectives on Psychological Science, 11(2), 265–279.CrossRefPubMedGoogle Scholar
  62. Pelowski, M., Markey, P. S., Forster, M., Gerger, G., & Leder, H. (2017). Move me, astonish me… delight my eyes and brain: The Vienna integrated model of top-down and bottom-up processes in art perception (VIMAP) and corresponding affective, evaluative, and neurophysiological correlates. Physics of Life Reviews, 21, 80–125.CrossRefPubMedGoogle Scholar
  63. Perry, A., Saunders, S. N., Stiso, J., Dewar, C., Lubell, J., Meling, T. R., … Knight, R. T. (2017). Effects of prefrontal cortex damage on emotion understanding: EEG and behavioural evidence. Brain, 140(4), 1086–1099.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Pitcher, D. (2014). Facial expression recognition takes longer in the posterior superior temporal sulcus than in the occipital face area. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 34, 9173–9177.CrossRefGoogle Scholar
  65. Pitcher, D., Charles, L., Devlin, J. T., Walsh, V., & Duchaine, B. (2009). Triple dissociation of faces, bodies, and objects in extrastriate cortex. Current Biology, 19(4), 319–324.CrossRefPubMedGoogle Scholar
  66. Pitcher, D., Garrido, L., Walsh, V., & Duchaine, B. C. (2008). Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. Journal of Neuroscience, 28(36), 8929-8933.CrossRefPubMedGoogle Scholar
  67. Pitcher, D., Japee, S., Rauth, L., & Ungerleider, L. G. (2017). The superior temporal sulcus is causally connected to the amygdala: A combined TBS-fMRI study. Journal of Neuroscience, 37(5), 1156–1161.CrossRefPubMedGoogle Scholar
  68. Pourtois, G., Sander, D., Andres, M., Grandjean, D., Reveret, L., Olivier, E., & Vuilleumier, P. (2004). Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals. European Journal of Neuroscience, 20(12), 3507–3515.CrossRefPubMedGoogle Scholar
  69. Prime, S. L., Vesia, M., & Crawford, J. D. (2009). TMS over human frontal eye fields disrupts trans-saccadic memory of multiple objects. Cerebral Cortex, 20(4), 759–772.CrossRefPubMedGoogle Scholar
  70. Redies, C. (2015). Combining universal beauty and cultural context in a unifying model of visual aesthetic experience. Frontiers in Human Neuroscience, 9, 218.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Redies, C., Hänisch, J., Blickhan, M., & Denzler, J. (2007). Artists portray human faces with the Fourier statistics of complex natural scenes. Network, 18, 235–248.CrossRefPubMedGoogle Scholar
  72. Robertson, E. M., Theoret, H., & Pascual-Leone, A. (2003). Studies in cognition: The problems solved and created by transcranial magnetic stimulation. Journal of Cognitive Neuroscience, 15(7), 948–960.CrossRefPubMedGoogle Scholar
  73. Rossi, S., Hallett, M., Rossini, P. M., & Pascual-Leone, A. (2011). Screening questionnaire before TMS: An update. Clinical Neurophysiology, 122(8), 1686.CrossRefPubMedGoogle Scholar
  74. Rychlowska, M., Cañadas, E., Wood, A., Krumhuber, E. G., Fischer, A., & Niedenthal, P. M. (2014). Blocking mimicry makes true and false smiles look the same. PLOS ONE, 9(3), e90876.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Sakuta, Y., Kanazawa, S., & Yamaguchi, M. K. (2014). Shedding light on painters’ implicit knowledge: The effect of lighting on recognizing expression and facial impressions of a depicted person in portraits. Japanese Psychological Research, 56(3), 288–295.Google Scholar
  76. Schweinhart, A. M., & Essock, E. A. (2013). Structural content in paintings: Artists overregularize oriented content of paintings relative to the typical natural scene bias. Perception, 42(12), 1311–1332.CrossRefPubMedGoogle Scholar
  77. Srinivasan, R., Golomb, J. D., & Martinez, A. M. (2016). A neural basis of facial action recognition in humans. Journal of Neuroscience, 36(16), 4434–4442.CrossRefPubMedGoogle Scholar
  78. Umiltá, M. A., Berchio, C., Sestito, M., Freedberg, D., & Gallese, V. (2012). Abstract art and cortical motor activation: An EEG study. Frontiers in Human Neuroscience, 6, 311.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Vartanian, O., & Goel, V. (2004). Neuroanatomical correlates of aesthetic preference for paintings. Neuroreport, 15(5), 893–897.CrossRefPubMedGoogle Scholar
  80. Vartanian, O., & Skov, M. (2014). Neural correlates of viewing paintings: Evidence from a quantitative meta-analysis of functional magnetic resonance imaging data. Brain and Cognition, 87, 52–56.CrossRefPubMedGoogle Scholar
  81. Wang, S., Yu, R., Tyszka, J. M., Zhen, S., Kovach, C., Sun, S., … Mamelak, A. N. (2017). The human amygdala parametrically encodes the intensity of specific facial emotions and their categorical ambiguity. Nature Communications, 8, 14821.CrossRefPubMedPubMedCentralGoogle Scholar
  82. Winston, J. S., O’Doherty, J., & Dolan, R. J. (2003). Common and distinct neural responses during direct and incidental processing of multiple facial emotions. NeuroImage, 20(1), 84–97.CrossRefPubMedGoogle Scholar
  83. Wood, A., Rychlowska, M., Korb, S., & Niedenthal, P. (2016). Fashioning the face: Sensorimotor simulation contributes to facial expression recognition. Trends in Cognitive Sciences, 20(3), 227–240.CrossRefPubMedGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2018

Authors and Affiliations

  • Chiara Ferrari
    • 1
  • Susanna Schiavi
    • 1
  • Zaira Cattaneo
    • 1
    • 2
  1. 1.Department of PsychologyUniversity of Milano-BicoccaMilanoItaly
  2. 2.IRCCS Mondino FoundationPaviaItaly

Personalised recommendations