Neural substrates associated with humor processing
© Noh et al.; licensee Springer. 2014
Received: 2 December 2013
Accepted: 10 January 2014
Published: 29 April 2014
Humor is composed of a cognitive element related to the detection of humor and an affective element related to the appreciation of humor. To investigate activated areas of the brain related to the two components of humor and to identify neural substrates associated with the degree of humor intensity, 13 participants were scanned while watching cartoons.
While watching humorous scenes, various areas of the brain were activated, including (1) the inferior gyrus, an area involved in reconciling ambiguous semantic content with stored knowledge, and (2) the temporal gyrus and fusiform gyrus, brain regions associated with the feeling of mirth. Further, humor intensity was positively correlated with BOLD signal magnitude in the nucleus accumbens, a region known to be involved in psychologically and psychopharmacologically driven rewards.
Our findings demonstrate a two-component neural circuit model of humor processing and a key region important in pleasurable feelings accompanied by humor.
Humor plays a central and unique role in human life. Without humor, life would undeniably be less exhilarating. Humor provides an effective means of communicating ideas, attracting partners, boosting mood, and even coping in times of trauma and stress (Brownell and Gardner ; Dixon ; Garilovic et al. ; Martin ; Mobbs et al. ; Neuhoff and Schaefer ; Nezlek and Derks ).
Humor involves both cognitive and affective elements (Gardner et al. ). The cognitive element refers to ‘getting the joke’ which includes moments during which the perceiver attempts to comprehend disparities between a punch line and prior experience (Brownell et al. ). The affective element refers to ‘enjoying a joke’; these are moments during which the perceiver experiences pure visceral, emotional responses depending on the hilarity of the experience (Shammi and Stuss ).
Studies have been conducted to identify biological neural systems related to humor. Gardner et al. () examined patients with brain injury. They found that the left hemisphere of the brain is related to the integration of information that is required for understanding humor and that the right hemisphere is associated with the emotional processing of humor. In another study, patients with an injury in the right hemisphere showed a low physical reaction and emotional response to humor (Shammi and Stuss ).
Studies comparing activated areas of the brain responsible for the affective element and the cognitive element have also been conducted. Moran et al. () examined a brain region that is activated during humor detection (cognitive element) and humor appreciation (affective element). The inferior frontal gyrus and posterior middle temporal gyrus were found to be activated during humor detection condition, while the insula and amygdala were activated during humor appreciation condition.
While numerous studies have focused on block-designed functional magnetic resonance imaging (fMRI) related to humor, few studies have explored event-related fMRI. Whether emotion-inducing stimuli should be presented in a block-designed paradigm or event-related paradigm during fMRI remains controversial. Block-designed paradigms are often used because of their easy implementation and because randomization, jittering, and spacing of different stimulus categories is not necessary (Josephs et al. ). In blocked designs, stimulus presentation is lengthened and consecutive stimuli in a block are predictable (Zarahn et al. ). Prolonged exposure of stimuli may decrease emotional involvement and hence alter underlying brain activation. In emotion research, presentation duration is particularly important, not only from a methodological point of view but also in respect of differences in information processing (Buhler et al. ). Event-related designs are superior in terms of rapid estimation of the hemodynamic response function to a short stimulus and are useful for emotion experiments, in part because of their ability to avoid the effects of confounding factors, such as habituation and anticipation (Rosen et al. ). In this study, we examined differences in brain activation associated with the two elements of humor, the cognitive element and the affective element, and identified brain areas positively correlated with the rating of funniness using an event-related fMRI paradigm.
Availability and requirements
Thirteen healthy, right-handed subjects participated in the experiment (mean age 24.8 ± 3.8 years, range 23−33 years, four men and nine women). No participant had a history of psychiatric or neurological disorders. The subjects were instructed to watch cartoons without laughing and to not move their heads.
Five cartoons were used in this study. All images were selected from a pilot study. The cartoons consisted of 7, 8, 9, 11, or 13 scenes. For fMRI study, cartoons were displayed on a monitor and presented to the subject through a 45° angled mirror positioned above the head coil.
fMRI experiments were conducted using an ISOL 3 T Forte scanner (ISOL Technology, Gyeonggi, Korea). During the presentation of visual stimuli, fMRI scanning was performed with the single shot Echo Planar Imaging sequence (repetition time (TR), 2,000 ms; echo time (TE), 28 ms; flip angle, 80°; field of view (FOV), 240 mm; matrix size, 64 × 64; slice thickness, 5 mm, no gap; and in-plane resolution, 3.75 mm, three dummy scans). Anatomical T1-weighted images were obtained with a 3-D FLAIR sequence (TR 280, TE 14, FA 60, FOV 240, matrix 256 × 256, 4-mm slice thickness).
Functional images were analyzed using SPM99 (http://www.fil.ion.ucl.ac.uk/spm/software/spm99/). Data including head motion artifacts that could not be corrected were excluded from analysis. All functional images were realigned with six movement parameters (translation; x, y, z and rotation; pitch, roll, yaw) to correct head motion. Echo-planar imaging (EPI) and T1-weighted images were coregistered and spatially normalized to the Montreal Neurological Institute template (MNI template) using an automated spatial transformation. Normalized images were smoothed using a 7-mm isotropic Gaussian kernel.
Following preprocessing, statistical analysis was performed. fMRI data were analyzed for each subject individually in the context of the general linear model (GLM) and theory of Gaussian random fields. Using subtraction and correlation procedures, activated areas in the brain while observing different pictures were color-coded by T-score.
Results and discussion
Humor detection is critically dependent upon resolving incongruities between punch lines and expectations shaped by the storyline (Sul ). Consistent with this notion, frontal regions engaged during humor detection have been implicated in language tasks that encourage the retrieval and appraisal of relevant semantic knowledge (Binder et al. , Price et al. ). Recent studies have indicated further specialization within the left inferior frontal cortex for reconciling ambiguous semantic content with stored knowledge (Gold and Buckner , Thompson-Schill et al. ). Inferior frontal regions may resolve ambiguities between these expectations and punch lines.
Activation of the fusiform gyrus and anterior temporal region caused by electrical stimulation induced laughter accompanied by a feeling of mirth (i.e., positive emotion; Arroyo et al. ). The temporal area, including the temporoparietal junction, is involved in the integration of multisensory information and coherence building and inferring knowledge (Ferstl and von Cramon ; Goel et al. ). Additionally, the temporal lobe may contribute to generating, testing, and correcting internal prediction regarding external sensory events, which is crucial for resolving incongruity in humor processing (Samson et al. ). These regions may be involved in the incongruent or surprising (Brownell et al. ) elements of a joke and thus may play a pivotal role in the early stages of the humor network.
The nucleus accumbens has been implicated in psychologically and psychopharmacologically driven rewards in various studies (Breiter et al. ; Knutson et al. ). Activation of the nucleus accumbens elicited by humor converges with findings from fMRI studies across a number of psychologically rewarding tasks, suggesting that this structure is involved in processing a diverse number of stimuli with rewarding characteristics (Aharon et al. ; Breiter et al. ; Erk et al. ; Rilling et al. ). Additionally, electrical stimulation of the nucleus accumbens results in laughter and giddiness (Okun et al. ). Although we cannot exclude other intervening factors (e.g., novelty), given the results of prior fMRI and physiological studies implicating the nucleus accumbens modulation in self-reported happiness (Knutson et al. ) and cocaine/amphetamine-induced euphoria in humans (Brieiter et al. ; Drevets et al. ), it is reasonable to conclude that nucleus accumbens activation observed in this study reflects the hedonic feeling accompanying humor.
In this study, using event-related fMRI, we identified areas of the brain that were activated during humor processing. We have presented evidence for differential systems underlying the cognitive and affective processes of humor and the brain region correlated with the degree of humor intensity.
This research has been supported by the Converging Research Center Program funded by the Ministry of Education, Science and Technology (2013K000332), the Korea Science and Engineering Foundation (No. 20120006577), and the Korea Basic Science Institute (T33408).
- Aharon I, Etcoff N, Ariely D, Chabris CF, O’Connor E, Breiter HC: Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron 2001, 32(3):537–551. 10.1016/S0896-6273(01)00491-3View ArticleGoogle Scholar
- Arroyo S, Lesser RP, Gordon B, Uematsu S, Hart H, Schwerdt P, Andeasson K, Fisher RS: Mirth, laughter and gelastic seizures. Brain 1993, 116(4):757–780. 10.1093/brain/116.4.757View ArticleGoogle Scholar
- Binder JR, Frost JA, Hammeke TA, Cox RW, Rao SM, Preieto T: Human brain language areas identified by functional magnetic resonance imaging. J Neurosci 1997, 17(1):353–362.Google Scholar
- Breiter HC, Aharon I, Kahneman D, Dale A, Shizgal P: Functional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron 2001, 30: 619–639. 10.1016/S0896-6273(01)00303-8View ArticleGoogle Scholar
- Brownell HH, Gardner H: Neuropsychological insights into humour. In Laughing matters: a serious look at humour. Edited by: Durant J, Miller J. Longman Scientific and Technia, Harlow, UK; 1988.Google Scholar
- Brownell HH, Michel D, Powelson J, Gardner H: Surprise but not coherence: sensitivity to verbal humor in right-hemisphere patients. Brain Language 1983, 18: 20–27. 10.1016/0093-934X(83)90002-0View ArticleGoogle Scholar
- Buhler M, Klein SV, Klemen J, Smolka MN (2008) Does erotic stimulus presentation design affect brain activation patterns? Event-related vs. blocked fMRI designs. Behav Brain Funct 4(1):30View ArticleGoogle Scholar
- Dixon NF (1980) Humor: A cognitive alternative to stress. In Spielberger CD, Sarason IG (eds) Anxiety and stress, Hemisphere, Washington DCGoogle Scholar
- Drevets WC, Gautier C, Price JC, Kupfer DJ, Kinahan PE, Grace AA, Price JL, Mathis CA: Amphetamine-induced dopamine release in human ventral striatum correlates with euphoria. Society of Biological Psychiatry 2001, 49: 81–96. 10.1016/S0006-3223(00)01038-6View ArticleGoogle Scholar
- Erk S, Spitzer J, Wunderlich AP, Galley L, Walter H: Cultural objects modulate reward circuitry. Neuroreport 2002, 13: 2499–2503. 10.1097/00001756-200212200-00024View ArticleGoogle Scholar
- Ferstl EC, von Cramon DY: What does the frontomedian cortex contribute to language processing: coherence or theory of mind? Neuroimage 2002, 17: 1599–1612. 10.1006/nimg.2002.1247View ArticleGoogle Scholar
- Gardner H, Ling PK, Flamm L, Silverman J: Comprehension and appreciation of humorous material following brain damage. Brain 1975, 98: 399–412. 10.1093/brain/98.3.399View ArticleGoogle Scholar
- Gavrilobic J, Lecic-Tosevski D, Dimic S, Pejovic-Milovancevic M, Knezevic G, Priebe S: Coping strategies in civilians during air attacks. Soc Psychiatry Psychiatr Epidemiol 2003, 38(3):128–133. 10.1007/s00127-003-0612-9View ArticleGoogle Scholar
- Goel V, Grafman JNS, Sadato N, Hallett M: Modeling other minds. Neuroreport 1995, 6: 1741–1746. 10.1097/00001756-199509000-00009View ArticleGoogle Scholar
- Gold BT, Buckner RL: Common prefrontal regions coactivate with dissociable posterior regions during controlled semantic and phonological task. Neuron 2002, 35(4):803–812. 10.1016/S0896-6273(02)00800-0View ArticleGoogle Scholar
- Josephs O, Turner R, Friston K: Event-related fMRI. Hum Brain Mapp 1997, 5: 243–248. 10.1002/(SICI)1097-0193(1997)5:4<243::AID-HBM7>3.0.CO;2-3View ArticleGoogle Scholar
- Knutson B, Adams CM, Fong GW, Hommer D: Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 2001, 21: RC159.Google Scholar
- Martin RA: Humor, laughter, and physical health: methodological issues and research findings. Psychol Bull 2001, 127(4):504–519. 10.1037/0033-2909.127.4.504View ArticleGoogle Scholar
- Mobbs D, Grecius MD, Abdel-Azim E, Menon V, Reiss AL: Humor modulates the mesolimbic reward centers. Neuron 2003, 40: 1041–1048. 10.1016/S0896-6273(03)00751-7View ArticleGoogle Scholar
- Moran JM, Wig GS, Adams RB, Janata P, Kelley WM: Neural correlates of humor detection and appreciation. Neuroimage 2004, 21(3):1055–1060. 10.1016/j.neuroimage.2003.10.017View ArticleGoogle Scholar
- Netzlek JB, Derks P: Use of humor as a copying mechanism, psychological adjustment, and social interaction. Humor International Journal of Humor Research. 2001, 14: 395–413.Google Scholar
- Neuhoff CC, Scahaefer C: Effects of laughing, smiling, and howling on mood. Psychol Rep. 2002, 91: 1079–1080. 10.2466/pr0.2002.91.3f.1079View ArticleGoogle Scholar
- Okun MS, Bowers D, Springer U, Shapira NA, Malone D, Rezai AR, Nuttin B, Heilman KM, Morecraft RJ, Rasmussen SA, Greenberg BD, Foote KD, Goodman WK: What’s in a smile? Intra-operative observation of contralateral smiles induced by deep brain stimulation. Neurocase 2004, 10(4):271–279. 10.1080/13554790490507632View ArticleGoogle Scholar
- Price CJ, Green DW, von Studnitz RA: Functional imaging study of translation and language switching. Brain 1999, 122(12):2221–2235. 10.1093/brain/122.12.2221View ArticleGoogle Scholar
- Rilling JK, Gutman DA, Zeh TR, Pagnoni G, Berns GS, Kilts CD: A neural basis for social cooperation. Neuron 2002, 35(2):395–405. 10.1016/S0896-6273(02)00755-9View ArticleGoogle Scholar
- Rosen BR, Buckner RL, Dale AM: Event-related functional MRI: past, present and future. PNAS Proc Natl Acad Sci U S A 1998, 95(3):773–780. 10.1073/pnas.95.3.773View ArticleGoogle Scholar
- Samson AC, Hempelmann CF, Huber O, Zysset S: Neural substrates of incongruity-resolution and nonsense humor. Neuropsychologia 2009, 47: 1023–1033. 10.1016/j.neuropsychologia.2008.10.028View ArticleGoogle Scholar
- Shammi P, Stuss DT: Humour appreciation: a role of the right frontal lobe. Brain 1999, 122: 657–666. 10.1093/brain/122.4.657View ArticleGoogle Scholar
- Shammi P, Stuss DT: The effects of normal aging on humor appreciation. J Int Neuropsychol Soc 2003, 9: 855–863.View ArticleGoogle Scholar
- Suls J: A two-stage model for the appreciation of jokes and cartoons. In The psychology of humor: theoretical perspectives and empirical issue. Edited by: Goldstein PE, McGhee JH. Thieme Medical Publishers, New York; 1972:81–100. 10.1016/B978-0-12-288950-9.50010-9View ArticleGoogle Scholar
- Thompson-Schill SL, E’Esposito M, Aguirre GK, Farah M: Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. PNAS 1997, 94(26):14792–14797. 10.1073/pnas.94.26.14792View ArticleGoogle Scholar
- Zarahn E, Aguirre G, D’Esposito M: A trial-based experimental design for fMRI. Neuroimage 1997, 6: 122–138. 10.1006/nimg.1997.0279View ArticleGoogle Scholar
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