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/lp/springer-journals/neural-substrates-associated-with-humor-processing-XczyA56KT7
- Publisher
- Springer Journals
- Copyright
- 2014 Noh et al.; licensee Springer.
- eISSN
- 2093-3371
- DOI
- 10.1186/s40543-014-0020-7
- Publisher site
- See Article on Publisher Site
Abstract
Background: 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. Findings: 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. Conclusions: Our findings demonstrate a two-component neural circuit model of humor processing and a key region important in pleasurable feelings accompanied by humor. Keywords: Emotion; Humor; Detection; Appreciation; Event-related fMRI Findings Studies have been conducted to identify biological Humor plays a central and unique role in human life. neural systems related to humor. Gardner et al. (1975) Without humor, life would undeniably be less exhilarating. examined patients with brain injury. They found that the Humor provides an effective means of communicating left hemisphere of the brain is related to the integration ideas, attracting partners, boosting mood, and even coping of information that is required for understanding humor in times of trauma and stress (Brownell and Gardner and that the right hemisphere is associated with the emo- 1988; Dixon 1980; Garilovic et al. 2003; Martin 2001; tional processing of humor. In another study, patients with Mobbs et al. 2003; Neuhoff and Schaefer 2002; Nezlek and an injury in the right hemisphere showed a low physical Derks 2001). reaction and emotional response to humor (Shammi and Humor involves both cognitive and affective elements Stuss 1999). (Gardner et al. 1975). The cognitive element refers to Studies comparing activated areas of the brain respon- ‘getting the joke’ which includes moments during which sible for the affective element and the cognitive element the perceiver attempts to comprehend disparities between have also been conducted. Moran et al. (2004) examined a punch line and prior experience (Brownell et al. 1983). a brain region that is activated during humor detection The affective element refers to ‘enjoying a joke’; these are (cognitive element) and humor appreciation (affective moments during which the perceiver experiences pure element). The inferior frontal gyrus and posterior middle visceral, emotional responses depending on the hilarity temporal gyrus were found to be activated during humor of the experience (Shammi and Stuss 2003). 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 * Correspondence: jhsohn@cun.ac.kr humor, few studies have explored event-related fMRI. Department of Psychology, Brain Research Institute, Chungnam National University, Daejeon, South Korea Whether emotion-inducing stimuli should be presented Full list of author information is available at the end of the article in a block-designed paradigm or event-related paradigm © 2014 Noh et al.; licensee Springer. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Noh et al. Journal of Analytical Science and Technology 2014, 5:20 Page 2 of 6 http://www.jast-journal.com/content/5/1/20 during fMRI remains controversial. Block-designed para- (1 least funny, 7 most funny). The subjects were then digms are often used because of their easy implementation asked to explain the meaning of the cartoons (Figure 1). and because randomization, jittering, and spacing of different stimulus categories is not necessary (Josephs Image acquisition et al. 1997). In blocked designs, stimulus presentation fMRI experiments were conducted using an ISOL 3 T is lengthened and consecutive stimuli in a block are Forte scanner (ISOL Technology, Gyeonggi, Korea). predictable (Zarahn et al. 1997). Prolonged exposure of During the presentation of visual stimuli, fMRI scanning stimuli may decrease emotional involvement and hence was performed with the single shot Echo Planar Imaging alter underlying brain activation. In emotion research, sequence (repetition time (TR), 2,000 ms; echo time (TE), presentation duration is particularly important, not only 28 ms; flip angle, 80°; field of view (FOV), 240 mm; matrix from a methodological point of view but also in respect size, 64 × 64; slice thickness, 5 mm, no gap; and in-plane of differences in information processing (Buhler et al. resolution, 3.75 mm, three dummy scans). Anatomical 2008). Event-related designs are superior in terms of T1-weighted images were obtained with a 3-D FLAIR rapid estimation of the hemodynamic response func- sequence (TR 280, TE 14, FA 60, FOV 240, matrix tion to a short stimulus and are useful for emotion 256 × 256, 4-mm slice thickness). experiments, in part because of their ability to avoid the effects of confounding factors, such as habituation Data analysis and anticipation (Rosen et al. 1998). In this study, we Functional images were analyzed using SPM99 (http:// examined differences in brain activation associated www.fil.ion.ucl.ac.uk/spm/software/spm99/). Data includ- with the two elements of humor, the cognitive element ing head motion artifacts that could not be corrected were and the affective element, and identified brain areas excluded from analysis. All functional images were rea- positively correlated with the rating of funniness using ligned with six movement parameters (translation; x, y, z an event-related fMRI paradigm. and rotation; pitch, roll, yaw) to correct head motion. Echo-planar imaging (EPI) and T1-weighted images were Availability and requirements coregistered and spatially normalized to the Montreal Participants Neurological Institute template (MNI template) using Thirteen healthy, right-handed subjects participated in an automated spatial transformation. Normalized images the experiment (mean age 24.8 ± 3.8 years, range 23−33 were smoothed using a 7-mm isotropic Gaussian kernel. years, four men and nine women). No participant had a Following preprocessing, statistical analysis was per- history of psychiatric or neurological disorders. The sub- formed. fMRI data were analyzed for each subject indi- jects were instructed to watch cartoons without laughing vidually in the context of the general linear model and to not move their heads. (GLM) and theory of Gaussian random fields. Using subtraction and correlation procedures, activated areas in the brain while observing different pictures were Stimuli color-coded by T-score. 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 dis- Results and discussion played on a monitor and presented to the subject Behavioral results through a 45° angled mirror positioned above the head After fMRI experiments, all participants rated the intensity coil. of humor. The number of subjects who experienced humor while watching each cartoon was 9 for cartoon #1, 11 for cartoon #2, 8 for cartoon #3, 13 for cartoon #4, and Experimental design 8 for cartoon #5 (Figure 2, upper image). Participants Stimuli were presented by showing five cartoons selected who recognized the cartoons as funny reported an average from a pilot experiment. Stimuli were presented according of 3.5 points for cartoon #1, 3.2 points for cartoon #2, 2.5 to an event-related fMRI paradigm with each cartoon points for cartoon #3, 5.2 points for cartoon #4, and 1.9 beingpresented for32to46s.The subjects were points for cartoon #5, respectively (Figure 2, lower image). instructed to press a button on a keypad immediately if they found the cartoon to be funny. The interval between the cartoons was 4 s. Following the scan, each fMRI results subject was instructed to assess humor intensity. The While viewing humorous scenes, significant activation subjects were asked to state whether they found the was observed in the bilateral middle temporal gyrus, left cartoon funny. If they did find it funny, they were asked to superior temporal gyrus, right fusiform gyrus, right para- rate their perceived humor intensity on a scale of 1 to 7 hippocampal gyrus, left uncus, left inferior frontal gyrus, Noh et al. Journal of Analytical Science and Technology 2014, 5:20 Page 3 of 6 http://www.jast-journal.com/content/5/1/20 Figure 1 Experimental design. Total experiment time was 45 min, including briefing and psychological assessment. humor non-humor cartoon1 cartoon2 cartoon3 cartoon4 cartoon5 intensity cartoon1 cartoon2 cartoon3 cartoon4 cartoon5 Figure 2 Psychological assessment. Number of subjects who recognized cartoons as humorous or not humorous (upper image). Mean humor intensity of cartoons (lower image). Mean Humor Intensity Number of Subject Noh et al. Journal of Analytical Science and Technology 2014, 5:20 Page 4 of 6 http://www.jast-journal.com/content/5/1/20 Figure 3 Areas of the brain activated by humorous scenes. Bilateral middle temporal gyrus, left superior temporal gyrus, right fusiform gyrus, right parahippocampal gyrus, left uncus, left inferior frontal gyrus, and right middle frontal gyrus were activated while experiencing humor. Figure 4 Areas of the brain activated during cartoon scenes with different degrees of humor intensity. Activation in the left nucleus accumbens and right middle temporal gyrus is correlated with humor intensity. Noh et al. Journal of Analytical Science and Technology 2014, 5:20 Page 5 of 6 http://www.jast-journal.com/content/5/1/20 and right middle frontal gyrus (p < 0.001, uncorrected; observed in this study reflects the hedonic feeling accom- Figure 3). panying humor. Humor detection is critically dependent upon resolving incongruities between punch lines and expectations shaped Conclusions by the storyline (Sul 1972). Consistent with this notion, In this study, using event-related fMRI, we identified areas frontal regions engaged during humor detection have been of the brain that were activated during humor processing. implicated in language tasks that encourage the retrieval We have presented evidence for differential systems and appraisal of relevant semantic knowledge (Binder et al. underlying the cognitive and affective processes of 1997, Price et al. 1999). Recent studies have indicated humor and the brain region correlated with the degree further specialization within the left inferior frontal cortex of humor intensity. for reconciling ambiguous semantic content with stored knowledge (Gold and Buckner 2002, Thompson-Schill Competing interests The authors declare that they have no competing interests. et al. 1997). Inferior frontal regions may resolve ambi- guities between these expectations and punch lines. Authors' contributions Regression analysis was used to examine the association JN, JWS, JHS, and CC carried out fMRI experiments and analysis. JN and SHK between humor intensity (i.e., the degree of funniness as drafted the manuscript. All authors read and approved the final manuscript. rated by each subject) and BOLD signal magnitude. This Acknowledgements analysis revealed that humor intensity was associated This research has been supported by the Converging Research Center with increased activation in the left nucleus accumbens Program funded by the Ministry of Education, Science and Technology and right middle temporal gyrus (p < 0.001, uncorrected; (2013K000332), the Korea Science and Engineering Foundation (No. 20120006577), and the Korea Basic Science Institute (T33408). Figure 4). Activation of the fusiform gyrus and anterior temporal Author details region caused by electrical stimulation induced laughter Division of Magnetic Resonance Research, Korea Basic Science Institute, Ochang, Chungbuk, South Korea. Department of Psychology, Brain Research accompanied by a feeling of mirth (i.e., positive emotion; Institute, Chungnam National University, Daejeon, South Korea. Department Arroyo et al. 1993). The temporal area, including the of Professional Counseling and Psychotherapy, Graduate School of Health temporoparietal junction, is involved in the integration and Complementary Medicine, Wonkwang University, Iksan, Cheonbuk 570-749, South Korea. of multisensory information and coherence building and inferring knowledge (Ferstl and von Cramon 2002; Received: 2 December 2013 Accepted: 10 January 2014 Goel et al. 1995). 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Journal
"Journal of Analytical Science and Technology" – Springer Journals
Published: Dec 1, 2014
Keywords: Analytical Chemistry; Characterization and Evaluation of Materials; Monitoring/Environmental Analysis