Abstract
The cognitive processes involved in humor comprehension were analyzed by directly comparing the time course of brain activity associated with the perception of slapstick humor and that associated with the comprehension of humor requiring theory of mind (ToM). Four different comic strips (strips containing humorous scenes that required ToM, non-ToM humorous strips, non-humorous semantically coherent strips and non-humorous semantically incoherent strips) were presented to participants, while their EEG response was recorded. Results showed that both of the humorous comic strips and the semantically incongruent strip elicited an N400 effect, suggesting similar cognitive mechanisms underlying the processing of incongruent and humorous comic strips. The results also showed that the humorous ToM strips elicited a frontal late positive (LP) response, possibly reflecting the active deployment of ToM abilities such as perspective-taking and empathy that allow for the resolution and interpretation of apparently incongruent situations. In addition, the LP response was positively correlated with ratings of perceived amusement as well as individual empathy scores, suggesting that the increased LP response to ToM humorous strips reflects the combined activation of neural mechanisms involved in the experience of amusement and ToM abilities. Overall, humor comprehension appears to demand distinct cognitive steps such as the detection of incongruent semantic components, the construction of semantic coherence, and the appreciation of humoristic elements such as maladaptive emotional reactions. Our results show that the deployment of these distinct cognitive steps is at least partially dependent on individual empathic abilities.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00221-020-05753-7/MediaObjects/221_2020_5753_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00221-020-05753-7/MediaObjects/221_2020_5753_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00221-020-05753-7/MediaObjects/221_2020_5753_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00221-020-05753-7/MediaObjects/221_2020_5753_Fig4_HTML.png)
Similar content being viewed by others
References
Amoruso L, Gelormini C, Aboitiz F, González MA, Manes F, Cardona J, Ibanez A (2013) N400 ERPs for actions: building meaning in context. Front Hum Neurosci 2013:7
Attardo S, Hempelmann CF, DiMaio S (2002) Script oppositions and logical mechanisms: modeling incongruities and their resolutions. Humor Int J Humor Res 2002:15346
Bambini V, Bertini C, Schaeken W, Stella A, Russo FD (2016) Disentangling metaphor from context: an ERP study. Front Psychol 7:559
Bartolo A, Benuzzi F, Nocetti L, Baraldi P, Nichelli P (2006) Humor comprehension and appreciation: an FMRI study. J Cognit Neurosci 18(11):1789–1798
Bentin S, McCarthy G, Wood CC (1985) Event-related potentials, lexical decision, and semantic priming. Electroencephalogr Clin Neurophysiol 60:353–355
Bihrle AM, Brownell HH, Powelson JA, Gardner H (1986) Comprehension of humorous and nonhumorous materials by left and right brain-damaged patients. Brain Cogn 5:399–411
Bischetti L, Ceccato I, Lecce S, Cavallini E, Bambini V (2019) Pragmatics and theory of mind in older adults’ humor comprehension. Curr Psychol. https://doi.org/10.1007/s12144-019-00295-w
Brunet E, Sarfati Y, Hardy-Baylé MC, Decety J (2000) A PET investigation of the attribution of intentions with a nonverbal task. NeuroImage 11(2):157–166
Camblin CC, Ledoux K, Boudewy M, Gordon PC, Swaab TY (2007) Processing new and repeated names: effects of coreference on repetition priming with speech and fast RSVP. Brain Res 1146:172–184
Canal P, Bischetti L, Di S, Bertini C, Ricci I, Bambini V (2019) Brain and Cognition ‘Honey, shall I change the baby ? Well done, choose another one’: ERP and Time-Frequency correlates of humor processing. Brain and Cognit 132:1
Chan YC, Chou TL, Chen HC, Yeh YC, Lavallee JP, Liang KC, Chang KE (2013) Towards a neural circuit model of verbal humor processing: an fMRI study of the neural substrates of incongruity detection and resolution. NeuroImage 66:169–176
Cohn N, Paczynski M (2013) Prediction, events, and the advantage of agents: the processing of semantic roles in visual narrative. Cogn Psychol 67(3):73–97
Cohn N, Paczynski M, Jackendoff R, Holcomb PJ, Kuperberg GR (2012) (Pea)nuts and bolts of visual narrative: structure and meaning in sequential image comprehension. Cogn Psychol 65(1):1–38
Coulson S (2000) Semantic leaps: frame-shifting and conceptual blending in meaning construction. Cambridge University Press, Cambridge
Coulson S, Kutas M (2001) Getting it: human event-related brain response to jokes in good and poor comprehenders. Neurosci Lett 316(2):71–74
Coulson S, Van Petten C (2007) A special role for the right hemisphere in metaphor comprehension? ERP evidence from hemifield presentation. Brain Res 1146:128–145
Coulson S, Wu YC (2005) Right hemisphere activation of joke-related information: an event-related brain potential study. J Cognit Neurosci 17(3):494–506
Cuthbert BN, Schupp HT, Bradley MM, Birbaumer N, Lang PJ (2000) Brain potentials in affective picture processing: Covariation with autonomic arousal and affective report. Biol Psychol 52(2):95–111
De Oliveira Falcone M, Ferreira MC, Curty Monteiro da Luz R et al (2008) Inventário de Empatia (I.E.) desenvolvimento e validação de uma medida brasileira. Avaliaçao Psicol 7:321–334
Du X, Qin Y, Tu S, Yin H, Wang T, Yu C (2013) Differentiation of stages in joke comprehension: evidence from an ERP study. Int J Psychol 48(2):149–157
Feng Y, Chan Y, Chen H (2014) Specialization of neural mechanisms underlying the three-stage model in humor processing: an ERP study. J Neurolinguistics 32:59–70
Franklin RG, Adams RB (2011) The reward of a good joke: neural correlates of viewing dynamic displays of stand-up comedy. Cognit Affect Behav Neurosci 11(4):508–515
Geangu E, Gibson A, Kaduk K, Reid VM (2013) The neural correlates of passively viewed sequences of true and false beliefs. Soc Cognit Affect Neurosci 8(4):432–437
Goel V, Dolan RJ (2001) The functional anatomy of humor: segregating cognitive and affective components. Nat Neurosci 4(3):237–238
Gorenstein C, Andrade LHSG (1996) Validation of a Portuguese version of the beck depression inventory and the state-trait anxiety inventory in Brazilian subjects. Braz J Med Biol Res 29:453–457
Hagoort P, Brown C, Groothusen J (1993) The syntactic positive shift (sps) as an erp measure of syntactic processing. Lang Cognit Process 8(4):439–483
Hagoort P, Hald L, Bastiaansen KMP (2004) Integration of word meaning and world knowledge in language. Science 304:438–442
Happé F, Ehlers S, Fletcher P, Frith U, Johansson M, Gillberg C et al (1996) ‘Theory of mind’ in the brain. Evidence from a PET scan study of Asperger syndrome. NeuroReport 8:197–201
Iwase M, Ouchi Y, Okada H, Yokoyama C, Nobezawa S, Yoshi-kawa E, Tsukada H, Takeda M, Yamashita K, Takeda M et al (2002) Neural substrates of human facial expression of pleasant emotion induced by comic films: a PET study. NeuroImage17:758–768
Ku LC, Feng YR, Chan YC, Wu CL, Chen HC (2017) A re-visit of three-stage humor processing with readers' surprise, comprehension, and funniness ratings: an ERP study. J Neurolinguistics 42:49–62
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. https://doi.org/10.1146/annurev.psych.093008.131123
Kutas M, Hillyard SA (1980) Reading senseless sentences: brain potentials reflect semantic incongruity. Science 207:203–208
Kutas M, Hillyard SA (1984) Brain potentials during reading reflect word expectancy and semantic association. Nature 307:161–163
Liu D, Sabbagh MA, Gehring WJ, Wellman HM (2004) Decoupling beliefs from reality in the brain: an ERP study of theory of mind. NeuroReport 15:991–995
Liu D, Sabbagh MA, Gehring WJ, Wellman HM (2009) Neural correlates of children’s theory of mind development. Child Dev 80(2):318–326
Manfredi M, Adorni R, Proverbio AM (2014) Why do we laugh at misfortunes? An electrophysiological exploration of comic situation processing. Neuropychologia 61:324–334
Manfredi M, Proverbio AM, Gonçalves Donate A, Macarini S, De Araujo AM, Boggio PS (2017) tDCS application over the right STG improves facial expression recognition during humor detection. Exp Brain Res 2017:1–10
Manfredi M, Cohn N, De Araújo Andreoli M, Boggio PS (2018) Listening beyond seeing: event-related potentials to audiovisual processing in visual narrative. Brain Lang 2018:185
Manfredi M, Proverbio AM, Marques LM, Ribeiro B, Yumi Nakao Morello L, Boggio PS (2019) Anodal transcranial direct current stimulation of MPFC enhances humor processing. Soc Neurosci. https://doi.org/10.1080/17470919.2019.1674687
Manfredi M, Cohn N, Sanchez Mello P, Fernandez E, Boggio PS (2020) Visual and verbal narrative comprehension in children and adolescents with autism spectrum disorders: an ERP study. J Autism Dev Disord. https://doi.org/10.1007/s10803-020-04374-x
Marinkovic K, Baldwin S, Courtney MG, Witzel T, Dale AM, Halgren E (2011) Right hemisphere has the last laugh: neural dynamics of joke appreciation. Cognit Affect Behav Neurosci 11(1):113–130
Martin RA (2007) The psychology of humor. An integrative approach. Elsevier Academic Press, Burlington
Meinhardt J, Sodian B, Thoermer C, Döhnel K, Sommer M (2011) True- and false-belief reasoning in children and adults: an event-related potential study of theory of mind. Develop Cognit Neurosci 1:67–76
Mobbs D, Greicius MD, Abdel-Azim E, Menon V, Reiss AL (2003) Humor modulates the mesolimbic reward centers. Neuron 40(5):1041–1048
Moran JM, Wig GS, Adams RB, Janata P, Kelley WM (2004) Neural correlates of humor detection and appreciation. NeuroImage 21(3):1055–1060
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Osterhout L, Holcomb P (1992) Event-related potentials elicited by syntactic anomaly. J Mem Lang 31:758–806
Premack D, Woodruff G (1978) Does the chimpanzee have a theory of mind? Behav Brain Sci 1:515–526
Proverbio AM, Riva F (2009) RP and N400 ERP components reflect semantic violations in visual processing of human actions. Neurosci Lett 459:142–146
Regel S, Meyer L, Gunter TC (2014) Distinguishing neurocognitive processes reflected by P600 effects: evidence from ERPs and neural oscillations. PLoS One 9:e96840
Samson AC, Zysset S, Huber O (2008) Cognitive humor processing: different logical mechanisms in nonverbal cartoons—an fMRI study. Soc Neurosci 3:125–140
Schultz W (2002) Getting formal with dopamine and reward. Neuron 36(2):241–263
Shammi P, Stuss DT (1999) Humour appreciation: a role of the right frontal lobe. Brain J Neurol 122:657–666
Shibata M, Terasawa Y, Osumi T, Masui K, Ito Y, Sato A, Umeda S (2017) Time course and localization of brain activity in humor comprehension: an ERP/sLORETA study. Brain Res 1657:215–222
Sitnikova T, Kuperberg G, Holcomb PJ (2003) Semantic integration in videos of real-world events: an electrophysiological investigation. Psychophysiology 40(1):160–164
Sitnikova T et al (2008) Two neurocognitive mechanisms of semantic integration during the comprehension of visual real- world events. J Cognit Neurosci 20:2037–2057
Sitnikova T, Holcomb PJ, Kiyonaga KA, Kuperberg GR (2008) Two neurocognitive mechanisms of semantic integration during the comprehension of visual real-world events. J Cognit Neurosci 20(11):2037–2057
Spotorno N, Cheylus A, Van Der Henst JB, Noveck IA (2013) What’s behind a P600? Integration operations during irony processing. PLoS One 8:e66839
Suls J (1972) A two stage model for the appreciation of jokes and cartoons. In: Goldstein J, McGhee P (eds) Psychology of humor. Academic Press, New York
Tu S, Cao X, Yun X, Wang K, Zhao G, Qiu J (2014) A new association evaluation stage in cartoon apprehension: evidence from an ERP study. J Behav Brain Sci 2:75–83
Vissers CTWM, Virgillito D, Fitzgerald DA, Speckens AEM, Tendolkar I, van Oostrom I, Chwilla DJ (2010) The influence of mood on the processing of syntactic anomalies: evidence from P600. Neuropsychologia 48(12):3521–3531
Watson KK, Matthews BJ, Allman JM (2007) Brain activation during sight gags and language-dependent humor. Cereb Cortex 17(2):314–324
West WC, Holcomb PJ (2002) Event-related potentials during discourse-level semantic integration of complex pictures. Cognit Brain Res 13:363–375
Acknowledgements
Mirella Manfredi was supported by a FAPESP post-doctoral research Grant (2015/00553-5). Lucas M. Marques was supported by a FAPESP PhD Grant (2017/06136-2). William E. Comfort is supported by a FAPESP post-doctoral research Grant (2017/12752-8). Paulo S. Boggio is supported by a CNPq research Grant (311641/2015-6).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Melvyn A. Goodale.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Appendix A: Examples of comic strips
Appendix A: Examples of comic strips
5 congruent comic strips
5 incongruent comic strips
5 non-ToM humorous comic strips
5 ToM humorous comic strips
-
Rights and permissions
About this article
Cite this article
Manfredi, M., Proverbio, A.M., Sanchez Mello de Pinho, P. et al. Electrophysiological indexes of ToM and non-ToM humor in healthy adults. Exp Brain Res 238, 789–805 (2020). https://doi.org/10.1007/s00221-020-05753-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-020-05753-7