Neural Correlates of Contrast and Humor: Processing Common Features of Verbal Irony

Irony is a kind of figurative language used by a speaker to say something that contrasts with the context and, to some extent, lends humor to a situation. However, little is known about the brain regions that specifically support the processing of these two common features of irony. The present study had two main aims: (i) investigate the neural basis of irony processing, by delivering short ironic spoken sentences (and their literal counterparts) to participants undergoing fMRI; and (ii) assess the neural effect of two irony parameters, obtained from normative studies: degree of contrast and humor appreciation. Results revealed activation of the bilateral inferior frontal gyrus (IFG), posterior part of the left superior temporal gyrus, medial frontal cortex, and left caudate during irony processing, suggesting the involvement of both semantic and theory-of-mind networks. Parametric models showed that contrast was specifically associated with the activation of bilateral frontal and subcortical areas, and that these regions were also sensitive to humor, as shown by a conjunction analysis. Activation of the bilateral IFG is consistent with the literature on humor processing, and reflects incongruity detection/resolution processes. Moreover, the activation of subcortical structures can be related to the reward processing of social events.

[1]  Norihiro Sadato,et al.  Neural substrates of sarcasm: A functional magnetic-resonance imaging study , 2006, Brain Research.

[2]  Christian F. Hempelmann,et al.  Neural substrates of incongruity-resolution and nonsense humor , 2009, Neuropsychologia.

[3]  Raymond W. Gibbs,et al.  Emotional Reactions to Verbal Irony , 2000 .

[4]  Stefan Zysset,et al.  Cognitive humor processing: Different logical mechanisms in nonverbal cartoons—an fMRI study , 2008, Social neuroscience.

[5]  Herbert L. Colston,et al.  Contrast of Kind Versus Contrast of Magnitude: The Pragmatic Accomplishments of Irony and Hyperbole , 2000 .

[6]  Ingrid S. Johnsrude,et al.  The role of domain-general frontal systems in language comprehension: Evidence from dual-task interference and semantic ambiguity , 2010, Brain and Language.

[7]  Richard J. Gerrig,et al.  Additive Effects in the Perception of Sarcasm: Situational Disparity and Echoic Mention , 2000 .

[8]  Matthew H. Davis,et al.  Why Clowns Taste Funny: The Relationship between Humor and Semantic Ambiguity , 2011, The Journal of Neuroscience.

[9]  E. Kang,et al.  Neural Correlates of Bridging Inferences and Coherence Processing , 2012, Journal of psycholinguistic research.

[10]  Tai-Li Chou,et al.  Segregating the comprehension and elaboration processing of verbal jokes: An fMRI study , 2012, NeuroImage.

[11]  Herbert L. Colston,et al.  Contrast and pragmatics in figurative language: Anything understatement can do, irony can do better , 2000 .

[12]  T. Münte,et al.  Brain network of semantic integration in sentence reading: Insights from independent component analysis and graph theoretical analysis , 2014, Human brain mapping.

[13]  Patrizia Baraldi,et al.  Humor Comprehension and Appreciation: An fMRI Study , 2006, Journal of Cognitive Neuroscience.

[14]  Dorothee E. Mutschler,et al.  Neural correlates of irony comprehension: The role of schizotypal personality traits , 2010, Brain and Language.

[15]  Mirella Dapretto,et al.  Developmental changes in the neural basis of interpreting communicative intent. , 2006, Social cognitive and affective neuroscience.

[16]  R. Gibbs The Poetics of Mind: Figurative Thought, Language, and Understanding , 1994 .

[17]  Karl J. Friston,et al.  Conjunction revisited , 2005, NeuroImage.

[18]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[19]  Lindsey J. Powell,et al.  It's the Thought That Counts , 2006, Psychological science.

[20]  E. Bullmore,et al.  Common and Distinct Neural Substrates for Pragmatic, Semantic, and Syntactic Processing of Spoken Sentences: An fMRI Study , 2000, Journal of Cognitive Neuroscience.

[21]  Tokiko Harada,et al.  Distinction between the literal and intended meanings of sentences: A functional magnetic resonance imaging study of metaphor and sarcasm , 2012, Cortex.

[22]  Petr Janata,et al.  Neural correlates of humor detection and appreciation , 2004, NeuroImage.

[23]  M. Dapretto,et al.  Neural basis of irony comprehension in children with autism: the role of prosody and context. , 2006, Brain : a journal of neurology.

[24]  Penny M. Pexman,et al.  Context Incongruity and Irony Processing , 2003 .

[25]  S. Fekete,et al.  Irony comprehension and context processing in schizophrenia during remission – A functional MRI study , 2013, Brain and Language.

[26]  Jean E. Fox Tree,et al.  Recognizing Verbal Irony in Spontaneous Speech , 2002 .

[27]  E. Redcay The superior temporal sulcus performs a common function for social and speech perception: Implications for the emergence of autism , 2008, Neuroscience & Biobehavioral Reviews.

[28]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[29]  Rene Vohn,et al.  The subcortical role of language processing. High level linguistic features such as ambiguity-resolution and the human brain; an fMRI study , 2008, NeuroImage.

[30]  Reginald B. Adams,et al.  The reward of a good joke: neural correlates of viewing dynamic displays of stand-up comedy , 2011, Cognitive, affective & behavioral neuroscience.

[31]  J. Cummings,et al.  Frontal-subcortical circuitry and behavior , 2007, Dialogues in clinical neuroscience.

[32]  Michael Erb,et al.  Where in the brain is nonliteral language? A coordinate-based meta-analysis of functional magnetic resonance imaging studies , 2012, NeuroImage.

[33]  H. Gardner,et al.  Comprehension and appreciation of humorous material following brain damage. , 1975, Brain : a journal of neurology.

[34]  Akira Utsumi,et al.  The role of prosody and context in sarcasm comprehension: Behavioral and fMRI evidence , 2016, Neuropsychologia.

[35]  Ted Sanders,et al.  The Role of Coherence Relations and Their Linguistic Markers in Text Processing , 2000 .

[36]  A. Toyomura,et al.  Neural substrates of irony comprehension: A functional MRI study , 2010, Brain Research.

[37]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[38]  C. Honey,et al.  Topographic Mapping of a Hierarchy of Temporal Receptive Windows Using a Narrated Story , 2011, The Journal of Neuroscience.

[39]  S. Attardo 7. Humor and irony in iteraction: from mode adoption to failure of detection , 2002 .

[40]  S. Caillies,et al.  Verbal irony processing: how do contrast and humour correlate? , 2014, International journal of psychology : Journal international de psychologie.

[41]  R. Kreuz,et al.  Why Do People Use Figurative Language? , 1994 .

[42]  E. Winner,et al.  Why not say it directly? The social functions of irony , 1995 .

[43]  Ryuta Kawashima,et al.  Irony comprehension: Social conceptual knowledge and emotional response , 2014, Human brain mapping.

[44]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[45]  D. Grandjean,et al.  Processing of emotional vocalizations in bilateral inferior frontal cortex , 2013, Neuroscience & Biobehavioral Reviews.

[46]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

[47]  J. Allman,et al.  Brain activation during sight gags and language-dependent humor. , 2007, Cerebral cortex.

[48]  R. Wyer,et al.  A theory of humor elicitation. , 1992, Psychological review.

[49]  W. Schultz Multiple reward signals in the brain , 2000, Nature Reviews Neuroscience.

[50]  M. Greicius,et al.  Humor Modulates the Mesolimbic Reward Centers , 2003, Neuron.

[51]  Jian Huang,et al.  Involvement of left inferior frontal gyrus in sentence-level semantic integration , 2009, NeuroImage.

[52]  Jérôme Prado,et al.  Neural evidence that utterance-processing entails mentalizing: The case of irony , 2012, NeuroImage.

[53]  Allan L. Reiss,et al.  The neural basis of humour processing , 2013, Nature Reviews Neuroscience.

[54]  Bernard Mazoyer,et al.  Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing , 2006, NeuroImage.

[55]  I. Poggi,et al.  Multimodal markers of irony and sarcasm , 2003 .

[56]  M. Just,et al.  Brain correlates of discourse processing: An fMRI investigation of irony and conventional metaphor comprehension , 2006, Neuropsychologia.