Skip to main content
SpringerLink
Log in

tDCS application over the STG improves the ability to recognize and appreciate elements involved in humor processing

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

An Erratum to this article was published on 18 May 2017

Abstract

The superior temporal gyrus (STG) has been found to play a crucial role in the recognition of actions and facial expressions and may, therefore, be critical for the processing of humorous information. Here we investigated whether tDCS application to the STG would modulate the ability to recognize and appreciate the comic element in serious and comedic situations of misfortune. To this aim, the effects of different types of tDCS stimulation on the STG were analyzed during a task in which the participants were instructed to categorize various misfortunate situations as “comic” or “not comic”. Participants underwent three different tDCS conditions: Anodal-right/Cathodal-left; Cathodal-right/Anodal-left; Sham. Images depicting people involved in accidents were grouped into three categories based on the facial expression of the victim: angry or painful (Affective); bewildered and funny (Comic); and images that did not contain the victim’s face (No Face). An improvement in mean reaction times in response to both the Comic and No Face stimuli was observed following Anodal-left/Cathodal-right stimulation when compared to sham stimulation. This suggests that this stimulation type reduced the reaction times to socio-emotional complex scenes, regardless of facial expression. The Anodal-right/Cathodal-left stimulation reduced the mean reaction times for Comic stimuli only, suggesting that specifically the right STG may be involved in facial expression recognition and in the appreciation of the comic element in misfortunate situations. These results suggest a functional hemispheric asymmetry in STG response to social stimuli: the left STG might have a role in a general comprehension of social complex situations, while the right STG may be involved in the ability to recognize and integrate specific emotional aspects in a complex scene.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adolphs R (2002) Neural systems for recognizing emotion. Curr Opin Neurobiol 12(2):169–177

    Article  CAS  PubMed  Google Scholar 

  • Allison T, Puce A, Mccarthy G (2000) Social perception from visual cues: role of the STS region. Trends Cogn Sci 4(7):267–278

    Article  CAS  PubMed  Google Scholar 

  • Andrews TJ, Ewbank MP (2004) Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. NeuroImage 23(3):905–913

    Article  PubMed  Google Scholar 

  • Bartolo A, Benuzzi F, Nocetti L, Baraldi P, Nichelli P (2006) Humor comprehension and appreciation: an FMRI study. J Cogn Neurosci 18(11):1789–1798

    Article  PubMed  Google Scholar 

  • Beyer F, Münte TF, Krämer UM (2013) Increased neural reactivity to socio-emotional stimuli links social exclusion and aggression. Biol Psychol 96:102–110

    Article  PubMed  Google Scholar 

  • Boggio PS, Rocha RR, da Silva MT, Fregni F (2008) Differential modulatory effects of transcranial direct current stimulation on a facial expression go-no-go task in males and females. Neurosci Lett 447(2–3):101–105

    Article  CAS  PubMed  Google Scholar 

  • Bolognini N, Rossetti A, Casati C, Mancini F, Vallar G (2011) Neuromodulation of multisensory perception: a tDCS study of the sound-induced flash illusion. Neuropsychologia 49(2):231–237

    Article  PubMed  Google Scholar 

  • Bonda E, Ostry D, Evans A (1996a) Specific Involvement of human parietal systems in the perception of biological motion and the amygdala. J Neurosci 76(11):3737–3744

    Google Scholar 

  • Bonda E, Petrides M, Ostry D, Evans A (1996b) Specific involvement of human parietal systems and the amygdala in the perception of biological motion. J Neurosci 16:3737–3744

    CAS  PubMed  Google Scholar 

  • Boorstin (1990). Making movies work: thinking like a filmmaker. Silman-James Press, Beverley Hills

    Google Scholar 

  • Bruce V (1983) Recognizing faces. Philos Trans R Soc Lond Ser B 302:423–436

    Article  CAS  Google Scholar 

  • Bruce V, Valentine T (1986) Semantic priming of familiar faces. Q J Exp Psychol Sect A 38(1): 125–150

    Article  Google Scholar 

  • Bruce V, Young A (1986) Understanding face recognition. Br J Psychol 77:305–327

    Article  PubMed  Google Scholar 

  • Bruce V, Young A (1998) The science of face perception. Oxford University Press, New York. In the eye of the beholder: the science of face perception.

    Google Scholar 

  • Brunet E, Sarfati Y, Hardy-Bayle MC, Decety J (2000) A PET investigation of the attribution of intentions with a nonverbal task. NeuroImage 11:157–166

    Article  CAS  PubMed  Google Scholar 

  • Brunoni AR, Amadera J, Berbel B, Volz MS, Rizzerio BG, Fregni F (2011) A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation. Int J Neuropsychopharmacol 14(8):1133–1145

    Article  PubMed  Google Scholar 

  • Buxbaum LJ, Kalénine S (2010) Action knowledge, visuomotor activation, and embodiment in the two action systems. Ann N Y Acad Sci 1191:201–218

    Article  PubMed  PubMed Central  Google Scholar 

  • Calder AJ, Young AW (2005) Understanding the recognition of facial identity and facial expression. Nat Rev Neurosci 6(8):641–651

    Article  CAS  PubMed  Google Scholar 

  • Candidi M, Stienen BMC, Aglioti SM, De Gelder (2015) Virtual lesion of right posterior superior temporal sulcus modulates conscious visual perception of fearful expressions in faces and bodies. Cortex 65:184–194

    Article  PubMed  Google Scholar 

  • Decety J, Grèzes J (1999) Neural mechanisms subserving the perception of human actions. Trends Cogn Sci 3(5):172–178

    Article  CAS  PubMed  Google Scholar 

  • Decety J, Grezes J, Costes N, Perani D et al (1997) Brain activity during observation of actions. Influence of action content and subject’s strategy. Brain 120:1763–1777

    Article  PubMed  Google Scholar 

  • Engell AD, Haxby JV (2007) Facial expression and gaze-direction in human superior temporal sulcus. Neuropsychologia 45(14):3234–3241

    Article  PubMed  Google Scholar 

  • Franklin RG Jr, Adams RB Jr (2011) The reward of a good joke: neural correlates of viewing dynamic displays of stand-up comedy. Cogn Affect Behav Neurosci 11(4):508–515

    Article  PubMed  Google Scholar 

  • Fregni F, Boggio PS, Nitsche M, Bermpohl F, Antal A, Feredoes E et al (2005) Anodal transcranial direct current stimulation of prefrontal cortex enhances working memory. Exp Brain Res 166:23–30

    Article  PubMed  Google Scholar 

  • Goel V, Dolan RJ (2001) The functional anatomy of humor: segregating cognitive and affective components. Nat Neurosci 4(3):237–238

    Article  CAS  PubMed  Google Scholar 

  • Haxby JV, Hoffman EA, Gobbini MI (2000) The distributed human neural system for face perception. Trends Cogn Sci 4(6):223–233

    Article  CAS  PubMed  Google Scholar 

  • Herwig U, Satrapi P, Schönfeldt-Lecuona C (2003) Using the international 10–20 EEG system for positioning of transcranial magnetic stimulation. Brain Topogr 16:95–99

    Article  PubMed  Google Scholar 

  • Hinojosa JA, Mercado F, Carretié L (2015) N170 sensitivity to facial expression: a meta-analysis. Neurosci Biobehav Rev 55:498–509

    Article  CAS  PubMed  Google Scholar 

  • Horstmann G, Bauland A (2006) Search asymmetries with real faces: testing the anger-superiority effect. Emotion 6(2):193–207

    Article  PubMed  Google Scholar 

  • Hurley MM, Dennett D, Adams RG (2011) Inside jokes: using humor to reverse-engineer the mind. The MIT Press, Cambridge, MA

    Google Scholar 

  • Ishai A (2008) Let’s face it: it’s a cortical network. NeuroImage 40(2): 415–419

    Article  PubMed  Google Scholar 

  • Jeong JW, Diwadkar VA, Chugani CD, Sinsoongsud P, Muzik O, Behen ME, Chugani DC (2011) Congruence of happy and sad emotion in music and faces modifies cortical audiovisual activation. NeuroImage 54(4): 2973–2782

    Article  PubMed  Google Scholar 

  • Koenigsberg HW, Fan J, Ochsner KN, Liu X, Guise K, Pizzarello S, Siever LJ (2010) Neural correlates of using distancing to regulate emotional responses to social situations. Neuropsychologia 48(6):1813–1822

    Article  PubMed  PubMed Central  Google Scholar 

  • Kohn N, Kellermann T, Gur RC, Schneider F, Habel U (2011) Gender differences in the neural correlates of humor processing: implications for different processing modes. Neuropsychologia 49(5):888–897

    Article  CAS  PubMed  Google Scholar 

  • Kutas M, Federmeier KD (2011) Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). Annu Rev Psychol 62:621–647

    Article  PubMed  PubMed Central  Google Scholar 

  • Labar KS, Crupain MJ, Voyvodic JT (2003) Dynamic perception of facial affect and identity in the human brain. Cereb Cortex 13:1023–1033

    Article  PubMed  Google Scholar 

  • Lavan N, Lima CF (2014) Neurocognitive mechanisms for vocal emotions: sounds, meaning, action. J Neurosci Off J Soc Neurosci 34(39):12950–12952

    Article  CAS  Google Scholar 

  • Luck SJ, Kappenman ES (2012). Oxford handbook of event-related potential components. Oxford University Press, New York

    Google Scholar 

  • Manfredi M, Adorni R, Proverbio AM (2014) Why do we laugh at misfortunes? An electrophysiological exploration of comic situation processing. Neuropsychologia 61:324–334

    Article  PubMed  Google Scholar 

  • Marinkovic K, Baldwin S, Courtney MG, Witzel T, Dale AM, Halgren E (2011) Right hemisphere has the last laugh: neural dynamics of joke appreciation. Cogn Affect Behav Neurosci 11(1), 113–130

    Article  PubMed  Google Scholar 

  • Marques LM, Lapenta OM, Merabet LB, Bolognini N, Boggio PS (2014) Tuning and disrupting the brain-modulating the McGurk illusion with electrical stimulation. Front Hum Neurosci 8:533

    Article  PubMed  PubMed Central  Google Scholar 

  • Mobbs D, Greicius MD, Abdel-Azim E, Menon V, Reiss AL (2003) Humor modulates the mesolimbic reward centers. Neuron 40(5):1041–1048

    Article  CAS  PubMed  Google Scholar 

  • Narumoto J, Okada T, Sadato N, Fukui K, Yonekura Y (2001) Attention to emotion modulates fMRI activity in human right superior temporal sulcus. Cogn Brain Res 12:225–231

    Article  CAS  Google Scholar 

  • Neely MN, Walter E, Black JM, Reiss AL (2012) Neural correlates of humor detection and appreciation in children. J Neurosci Off J Soc Neurosci 32(5):1784–1790

    Article  CAS  Google Scholar 

  • Nitsche MA, Liebetanz D, Antal A, Lang N, Tergau F, Paulus W (2003a) Modulation of cortical excitability by weak direct current stimulation technical, safety and functional aspects. Suppl Clin Neurophysiol 56:255–276

    Article  PubMed  Google Scholar 

  • Öhman A, Lundqvist D, Esteves F (2001) The face in the crowd revisited: a threat advantage with schematic stimuli. J Pers Soc Psychol 80:381–396

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychololgia 9:97–113

    Article  CAS  Google Scholar 

  • Pessoa L, Padmala S (2007) Decoding near-threshold perception of fear from distributed single-trial brain activation. Cerebral cortex 17(3):691–701

    Article  PubMed  Google Scholar 

  • Pinkham AE, Griffin M, Baron R, Sasson NJ, Gur RC (2010) The face in the crowd effect: anger superiority when using real faces and multiple identities. Emotion 10(1):141–146

    Article  PubMed  Google Scholar 

  • Pitcher D (2014) Facial expression recognition takes longer in the posterior superior temporal sulcus than in the occipital face area. J Neurosci 34:9173–9177

    Article  CAS  PubMed  Google Scholar 

  • Pitcher D, Garrido L, Walsh L, Duchaine BC (2008) Transcranial magnetic stimulation disrupts the perception and embodiment of facial expressions. J Neurosci 28(36):8929–8933

    Article  CAS  PubMed  Google Scholar 

  • Proverbio AM, Riva F, Zani A (2010) When neurons do not mirror the agent’s intentions: sex differences in neural coding of goal-directed actions. Neuropsychologia 48(5):1454–1463

    Article  PubMed  Google Scholar 

  • Proverbio AM, Paganelli L, Cappa SF, Canessa N, Perani D, Zani A (2011) Neural coding of cooperative vs. affective human interactions: 150 ms to code the action’s purpose. PLoS One 6(7):e22026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Proverbio AM, Crotti N, Manfredi M, Adorni R (2012) Who needs a referee? How incorrect basketball actions are automatically detected by basketball players’ brain. ScientificReports (Nature), 2: 883

    Google Scholar 

  • Proverbio AM, Calbi M, Manfredi M, Zani A (2014) Comprehending body language and mimics: an ERP and neuroimaging study on Italian actors and viewers. PLoS One 9(3):e91294

    Article  PubMed  PubMed Central  Google Scholar 

  • Ratner C (1989) A social constructionist critique of naturalistic theories of emotion. J Mind Behav 10:211–230

    Google Scholar 

  • Samson D, Apperly, a I, Chiavarino C, Humphreys GW (2008) Cognitive humor processing: different logical mechanisms in nonverbal cartoons—an fMRI study. Soc Neurosci 3(2):125–140

    Article  PubMed  Google Scholar 

  • Samson AC, Hempelmann CF, Huber O, Zysset S (2009) Neural substrates of incongruity-resolution and nonsense humor. Neuropsychologia 47:1023–1033

    Article  PubMed  Google Scholar 

  • Stein J (ed) (2002) The Random House Dictionary of the English Language: the Unabridged Edition, 2 Revised edition

  • Suls JM (1972) A two-stage model for the appreciation of jokes and cartoons. In: Goldstein PE, McGhee JH (eds) The psychology of humour. Theoretical perspectives and empirical issues. Academic Press, New York, pp 81–100

    Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotactic atlas of the human brain. Thieme Verlag, Stuttgart

    Google Scholar 

  • Vander Wyk BC, Hudac CM, Carter EJ, Sobel DM, Pelphrey KA (2016) Action Understanding in the superior temporal sulcus region. Psychol Sci 20(6):771–777

    Article  Google Scholar 

  • Vrticka P, Black JM, Reiss AL (2013) The neural basis of humour processing. Nat Rev Neurosci 14(12):860–868

    Article  CAS  PubMed  Google Scholar 

  • Wallbott HG (1988) In and out of context: influences of facial expression and context information on emotion attributions. Br J Soc Psychol 27:357–369

    Article  Google Scholar 

  • Watson KK, Matthews BJ, Allman JM (2007) Brain activation during sight gags and language-dependent humor. Cereb Cortex 17(2):314–324

    Article  PubMed  Google Scholar 

  • Winston JS, Henson RNA, Dolan RJ (2004) fMRI-adaptation reveals dissociable neural representations of identity and expression in face perception. J Neurophysiol 92:1830–1839

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Japee S, Nolan R, Chu C, Liu N, Ungerleider LG (2016) NeuroImage Face-selective regions differ in their ability to classify facial expression. NeuroImage 130:77–90

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Paulo S. Boggio is supported by a CNPq research Grant (311641/2015-6). Mirella Manfredi is supported by a FAPESP post-doctoral researcher Grant (2015/00553-5).

Author information

Authors and Affiliations

  1. Social and Cognitive Neuroscience Laboratory and Developmental Disorders Program, Center for Health and Biological Sciences, Mackenzie Presbyterian University, Rua Piaui, 181, São Paulo, 01241-001, Brazil

    Mirella Manfredi, Ana Paula Gonçalves Donate, Sofia Macarini Gonçalves Vieira, William Edgar Comfort, Mariana De Araújo Andreoli & Paulo Sérgio Boggio

  2. Department of Psychology, University of Milano-Bicocca, Milan, Italy

    Alice Mado Proverbio

Authors
  1. Mirella Manfredi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alice Mado Proverbio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana Paula Gonçalves Donate
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sofia Macarini Gonçalves Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. William Edgar Comfort
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mariana De Araújo Andreoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Paulo Sérgio Boggio
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mirella Manfredi.

Additional information

An erratum to this article is available at http://dx.doi.org/10.1007/s00221-017-4974-8.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Manfredi, M., Proverbio, A.M., Gonçalves Donate, A.P. et al. tDCS application over the STG improves the ability to recognize and appreciate elements involved in humor processing. Exp Brain Res 235, 1843–1852 (2017). https://doi.org/10.1007/s00221-017-4932-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-017-4932-5

Keywords

Search

Navigation