Neuropsychologia 65 (2014) 137–145

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Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia

Integration of cognitive and affective networks in humor comprehension Midori Shibata a,b,n, Yuri Terasawa b,c,d, Satoshi Umeda b,c a

Department of Psychology, Hokkaido University, Kita 10, Nishi 7, Kita-ku, Sapporo 060-0810, Japan Global Research Centre of Logic and Sensibility, Keio University, Tokyo 108-0073, Japan c Department of Psychology, Keio University, Tokyo 108-8345, Japan d Department of Psychophysiology, National Institute of Mental Health, National Center of Neurology and Psychiatry, Kodaira-shi, Tokyo, Japan b

art ic l e i nf o

a b s t r a c t

Article history: Received 18 April 2014 Received in revised form 22 September 2014 Accepted 17 October 2014 Available online 28 October 2014

Humor comprehension is a complex process that requires the detection and resolution of the incongruity, eliciting a positive feeling of mirth or reward. We conducted a functional magnetic resonance imaging (fMRI) study to identify the key factors involved in this complex process. To reduce the influence of other factors, we utilized a group of sentences that were nearly identical across conditions (i.e., the first two sentences and the punch line were identical, but the third sentence was different). We found that the punch line (target sentence) in the funny condition induced a perception of funniness and elicited greater activation in language and semantic neural networks, which have been implicated in comprehension processing (i.e., incongruity detection and resolution). We also found increased activation in the mesolimbic reward regions, which have been implicated in the experience of positive rewards in the funny condition. Psycho-physiological interaction analyses revealed that language and semantic regions, such as inferior frontal gyrus (IFG), middle temporal gyrus (MTG), superior temporal gyrus (STG), superior frontal gyrus (SFG), and inferior parietal lobule (IPL) are simultaneously activated during humor comprehension processing. These analyses also revealed that the right MTG, the left IPL, and IFG showed enhanced connectivity with the midbrain. Our findings suggest that these networks play a central role in incongruity detection and resolution, as well as in positive emotional response. & 2014 Elsevier Ltd. All rights reserved.

Keywords: Humor fMRI Emotion Reward

1. Introduction Humor is a phenomenon that is elicited by particular cognitive processes. The perception of humor is associated with a strong emotional response, laughter, and changes in the brain and body via the autonomic and endocrine systems (Panksepp, 1993). These complex processes in humor comprehension have been investigated by philosophers, psychologists, linguists, and other theorists. Famous theories of humor comprehension propose that humorous stimuli are processed in steps (Coulson and Kutas, 2001; Papousek et al., 2013; Shultz, 1976; Suls, 1972), such that initial information contained in humorous stimuli activates stored expectations or a script. Further information then leads to the detection of incongruence in the relation of the first script to another. To understand the punch line of a joke (either verbal jokes or visual jokes), this incongruity has to be at least partially resolved. For example, the incongruity-resolution model

n Corresponding author at: Department of Psychology, Hokkaido University, Kita 10, Nishi 7, Kita-ku, Sapporo, 060-0810 Japan. Tel./fax: þ 81 11 706 4804. E-mail address: [email protected] (M. Shibata).

http://dx.doi.org/10.1016/j.neuropsychologia.2014.10.025 0028-3932/& 2014 Elsevier Ltd. All rights reserved.

indicates that a joke setup causes the listener to make a prediction about the likely outcome (Suls, 1972). When the punch line does not conform to the prediction, the listener is surprised and looks for a cognitive rule that will make the punch line follow from the material in the joke setup. When this cognitive rule is found, the incongruity is removed, the joke is perceived as funny. Thus, this model suggests that joke comprehension and appreciation is essentially a sort of cognitive problem-solving task. Since humor is context-dependent, funniness results from the insightful integration of contradictory or incongruous ideas (Martin, 2007). Over the past decade, many neuroimaging studies have examined the neural substrates involved in humor comprehension (Bekinschtein et al., 2011; Chan et al., 2012a, 2012b; Franklin and Adams, 2011; Goel and Dolan, 2001, 2007; Marinkovic et al., 2011; Mobbs et al., 2003, 2005; Moran et al., 2004; Neely et al., 2012; Rapp et al., 2008; Samson et al., 2009, 2008; Vrticka et al., 2013a, 2013c; Watson et al., 2007; Wild et al., 2006). These studies can be classified into two main groups based on the stimulus modalities used in the experiments: visual and verbal. One study utilizing visual stimuli was conducted by Samson and her colleagues, who used incongruityresolution and nonsense cartoons to investigate the neural basis of

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incongruity-resolution processes. They found that the anterior medial prefrontal cortex, bilateral superior frontal gyri, and the temporoparietal junctions (TPJ) showed more activation during processing of incongruity-resolution than of nonsense cartoons. Thus, compared with the processing of nonsense cartoons, the processing of incongruity-resolution cartoons appears to require more integration of multi-sensory information, coherence building, and thus more organization of information. Additionally, the temporoparietal junction (TPJ) and prefrontal areas appear to be involved in humor comprehension processes. Neely et al. (2012) conducted an fMRI experiment with typically developing children using video clips. In their experiment, three types of stimuli were used: Funny, Positive (enjoyable but not funny), and Neutral (not intended to evoke any emotional response). The results indicated that the Funny versus Positive contrast showed greater activation in the more superior TOPJ regions (BA 22, 37, and 40). They suggested that TOPJ activation may be specific to humor processing (i.e., involved in the satisfaction of detecting and resolving the incompatible elements of humor). On the other hand, the study utilizing verbal stimuli demonstrated that semantic jokes induced activation in the bilateral posterior middle temporal gyrus and left inferior temporal gyrus, whereas phonological jokes induced activation in the left inferior temporal gyrus and left inferior frontal gyrus (Goel and Dolan, 2001). The study also suggested that a common component of humor is correlated with activity in the ventromedial prefrontal cortex, which is involved in reward processing. In addition, a recent study utilizing verbal stimuli examined distinct brain regions associated with the detection and resolution of incongruities using unfunny, nonsensical and funny stories (Chan et al., 2012b). They found that detection of incongruities was associated with greater activation in the right middle temporal gyrus and the right medial frontal gyrus. Additionally, the resolution of incongruities was associated with increased activation in the left inferior frontal gyrus, superior frontal gyrus and the left inferior parietal lobule. Based on their results, Chan and colleagues suggested a three-stage neural circuit model for verbal humor processing, which includes incongruity detection and incongruity resolution during humor comprehension, and feelings of amusement during humor elaboration. These findings indicate that humor comprehension entails complex cognitive affective interaction. Several recent studies have investigated the relationship between these cognitive and affective components (Amir et al., 2013; Kohn et al., 2011). To explore gender differences in humor comprehension, Kohn et al. (2011) conducted an fMRI experiment using online subjective funniness ratings for parametric modulation. They found different humor processing styles in men compared to women. The results of the parametric modulation analysis indicated that the amygdala, insula, and precuneus are involved in the affective state of understanding a joke. Amir et al. (2013) conducted fMRI experiment using the drawings that were uninterpretable prior to

the presentation of a caption (humorous interpretation or nonhumorous (or insight) interpretation). Their results indicated that humorous versus nonhumorous (insight) contrast showed greater activation in the temporal poles and temporo-occipital junction, TPJ, medial prefrontal cortex and reward regions. Based on their results, they hypothesized that neural activation in association cortex would be greater in response to novel, and surprising experiences, resulting in greater opioid release. Activity in these areas, which may facilitate the release of dopamine through reward pathways, may be experienced as pleasurable (Biederman and Vessel, 2006). Although the regions involved in the cognitive and affective processes underlying perception of humor have been identified in the studies discussed above, the interaction between these regions is unclear. To elucidate these interaction processes, we conducted a functional magnetic resonance imaging (fMRI) experiment to examine the relationship between these cognitive and affective components of humor. To isolate the key factors that enhance funniness, we used stimuli sentences that were nearly identical across conditions (i.e., the first two sentences and the punch line were identical, but the third sentence was different). As illustrated in Fig. 1, we used the same target sentences across conditions so that any differences between the funny and unfunny condition would be due to the neural mechanisms involved in humor comprehension processing. Based on the incongruity-resolution model (Suls, 1972) and the three-stage neural circuit model (Chan et al., 2012b), we hypothesized that the middle temporal gyrus (MTG), medial prefrontal cortex (MPFC), inferior frontal gyrus (IFG), superior frontal gyrus (SFG), and inferior parietal lobule (IPL) would play a key role in comprehension processing, such as incongruity detection and resolution. We also hypothesized that subcortical regions, including the hippocampus, amygdala, and midbrain play a key role in eliciting feeling of amusement. In addition to contrasting the signals obtained in the funny versus unfunny condition, we used psycho-physiological interaction (PPI) analyses to investigate the functional connectivity between the regions involved in cognitive affective interaction of humor comprehension. PPI analysis is a validated method to explain neural responses in one brain area in terms of the interaction between the influences of another brain region and a task condition (Friston et al., 1997; O’Reilly et al., 2012). Thus, we sought to investigate functional interactions among brain regions during humor comprehension, and to evaluate how humor comprehension elicited activity in the mesolimbic reward system. 2. Methods 2.1. Participants Twenty graduate and undergraduate students (15 women and five men; mean age¼ 22.5 years; range: 20–34) participated in this experiment. The participants did not have a history of mental or neurological disorders, and were all right-handed,

Fig. 1. Experimental paradigm. There were two experimental conditions: the funny and unfunny conditions. The first two sentences and the target sentence (punch line) were identical, while the third sentence differed between conditions. The stimuli were presented in an event-related fMRI paradigm. The analysis was limited to the bloodoxygenation level-dependent (BOLD) signal acquired for each onset point.

M. Shibata et al. / Neuropsychologia 65 (2014) 137–145 and native Japanese speakers. The experiment was performed with the approval of the Keio University Research Ethics Committee. All participants gave written informed consent prior to participation. 2.2. Stimuli Our experiment contained two experimental conditions: the funny and unfunny conditions. For the funny condition, we created 70 different scenarios (Nouchi, 2004). We also created 70 uninteresting scenarios for the unfunny condition, in which the first two sentences and the target sentence were identical to those in the funny scenarios, but the third sentence was different (Fig. 1). Prior to the fMRI experiment, these funny and unfunny scenarios were rated on a scale of 1 to 5 (1 ¼extremely unfunny, 5 ¼extremely funny) by 20 additional participants who were similar in age and background to the experimental participants (8 women and 12 men, mean age 25.79, S.D. ¼ 4.59). The 56 scenarios with the highest funniness ratings were selected for funny condition. We also selected 56 paired unfunny scenarios for unfunny condition (mean ratings for funny scenarios: 3.70, S. D. ¼ 0.41, mean ratings for unfunny scenarios: 2.30, S.D. ¼0.33). A one-way ANOVA yielded significant differences between the two experimental conditions for funniness ratings (F (1, 55) ¼ 389.10, p o 0.0001). All the words in the sentences were matched in terms of familiarity, frequency and word length. The sentences were matched in terms of context and could be understood literally. The important difference between funny and unfunny conditions was that the punch line (target sentence) in the funny condition induced the perception of incongruity. Accordingly, only the punch line (target sentence) in the funny condition induced a perception of funniness, despite the use of the same sentences in the unfunny condition. To ensure the homogeneity of the material, we created two counterbalanced lists based on the funniness ratings from the behavioral experiments, and presented list 1 to the first half of the participants and list 2 to the second half. Each list contained 28 funny scenarios and 28 unfunny scenarios. There were no significant differences in the funniness or non-funniness ratings between the two lists (funny scenarios; t(27) ¼0.37, p¼ 0.71, unfunny scenarios; t(27) ¼ 0.85, p¼ 0.40). Each pair of scenarios (funny/unfunny) was presented once in each list. 2.3. Procedures Before the scanning session, the participants completed a short practice set of trials from each condition to familiarize them with the task. The participants were instructed to press a “yes” button with their right index finger when they found the target sentence funny, and to press a “no” button with their right middle finger when they found the target sentence unfunny. The participants were also instructed not to move their heads if they laughed. The MRI scanning phase consisted of two sessions (328 functional image volumes per session). The trials were presented in a pseudo-random order. The first two sentences were presented for 9 s. The third sentence was presented for 4 s, and was immediately followed by the presentation of a fixation cross for 2 s. As soon as the target sentence (punch line) was presented (6 s), participants had to respond by pressing one of two buttons with their index finger if they found the target sentence funny, and the other button with their middle finger if they did not find the target sentence funny. The hand that was used for the button press was counterbalanced across participants. After the participant had made a selection, a fixation cross was presented for 6 s (Fig. 1). The presentation of the stimuli and the recording of participants' responses were controlled with E-prime (Psychology Software Tools, Inc.). Following the MRI scanning sessions, each participant was asked to rate each scenario that had been presented during the scanning session for humor intensity (i.e., degree of funniness) on a 1 to 5 scale (1 ¼ least funny, 5¼ most funny). Scenarios considered unfunny were given a zero. These subjective funniness ratings were then used to parametrically covary funniness with the associated linear changes in the BOLD signal intensity. In this post-scan questionnaire, each participant was asked a question regarding the predictability of the content of the target sentence (“Could you predict the ending of the scenario?”). 2.4. fMRI data acquisition and data analysis We used a Siemens Trio 3-T scanner was used to acquire high-resolution T1weighted anatomical images (1-mm isotropic resolution 3D MPRAGE) and gradient-echo EPIs with a blood oxygenation level-dependent (BOLD) contrast of 44 axial slices (descending). The parameters of the sequence were as follows: repetition time (TR) ¼2.35 s, echo time (TE) ¼30 ms, flip angle ¼901, voxel size ¼3.5  3.5  2 mm3, and slice gap ¼1 mm. A total of 656 scans were acquired per participant (328 volumes  2 sessions). The data were analyzed using SPM8 (http://www.fil.ion.ucl.ac.uk/spm). After correcting for differences in slice timing within each image volume (using the middle slice acquired in each time as a reference), corrections for head motion were made by realigning all functional volumes to the first volume of each participant. The volumes were subsequently coregistered with the anatomical image of each participant, spatially normalized to the Montreal Neurological Institute (MNI) brain template and smoothed using an 8-mm, full-width-at-half-maximum Gaussian kernel. After preprocessing, each participant's data were analyzed using the general linear model

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(Friston et al., 1997) implemented in SPM8. For the first two sentences, each trial was modeled as a boxcar, and convolved with a standard hemodynamic response function. Separate regressors were created for the two conditions (funny and unfunny). For the third sentence and the target sentence, an event-related design was employed. In addition, we corrected movement and signal artifacts using realignment parameters as additional regressors. We analyzed only the trials in which the participants choose the appropriate response (funny for the funny condition or non-funny for the non-funny condition). Subsequent second-level group random effects analyses were performed on the SPM contrast images of the first-level canonical HRF responses. The results of all second level analyses were initially thresholded at po0.001 (voxel-level, uncorrected). For the whole-brain search, further cluster-size statistics were used as the test statistics applying a threshold of family-wise error corrected (FWE) po0.05. We had a priori hypotheses about possible changes in the following regions: the middle temporal gyrus (MTG), medial prefrontal cortex (MPFC), inferior frontal gyrus (IFG), superior frontal gyrus (SFG), inferior parietal lobule (IPL) and mesolimbic reward regions (including the hippocampus, amygdala, ventral striatum, and midbrain) (Chan et al., 2012a, 2012b; Goel and Dolan, 2001, 2007; Mobbs et al., 2003; Vrticka et al., 2013c). We performed a small volume correction (SVC) on the anatomical ROI. ROIs of significance demonstrated clusters of activity that survived familywise error rate correction for multiple comparisons within these small volumes (Po0.05). Brain regions were identified from these x, v, and z coordinates using WFU PickAtlas software. 2.5. Psycho-physiological interaction (PPI) analysis We conducted psycho-physiological interaction (PPI) analyses (Friston et al., 1997; O’Reilly et al., 2012) to investigate the functional connectivity between the regions involved in the cognitive and affective components of humor appreciation. As mentioned above, Chan and colleagues proposed a three-stage neural circuit model for verbal humor processing, including incongruity detection (middle temporal gyrus and middle frontal gyrus) and incongruity resolution (inferior frontal gyrus, superior frontal gyrus, and inferior parietal lobule) during humor comprehension and inducement of the feeling of amusement during humor elaboration (Chan et al., 2012b). Based on the three-stage neural circuit model and the group data for the contrast of funny versus unfunny conditions (Table 1), we defined four seed regions (i.e., the right middle temporal gyrus (x¼58, y¼  4, z¼  22; BA 21), the left inferior frontal gyrus/Insula (x¼  36, y¼18, z¼  14; BA 47), the left superior frontal gyrus (x¼  14, y¼38, z¼ 44), and the left inferior parietal lobule (x¼  56, y¼  48, z¼52; BA 40) for evaluating how humor comprehension elicited activity in the mesolimbic reward system. We extracted the time series from a 6-mm radius sphere around the peak coordinates. The analysis consists of three regressors: the psychological vector that represents the contrast of two conditions (funny versus unfunny); the physiological vector that represents the time course of the seed region; and the interaction term of these two. The PPI was created for each participant by multiplying the deconvolved and mean-corrected BOLD signal with the psychological vector. After convolution with the hemodynamic response function (HRF), three regressors were entered in the statitistical analysis to determine conditiondependent changes of functional connectivity. The models were estimated, and contrasts were generated to test the effect of the PPIs that were used for the secondlevel analysis. In the second-level random-effects analysis, we used one-sample t-tests to identify the brain regions that showed increased or decreased connectivity with the seed regions. The results of PPI analyses are shown as significant after small volume correction on the anatomical regions of interest.

3. Results 3.1. Behavioral results In the scanner, participants pressed a “yes” button when they found the target sentence funny. They rated an average of 69.676.9% of the funny trials as subjectively funny. They also pressed a “no” button when they found the target sentence unfunny, and rated an average of 71.475.3% of the unfunny trials as subjectively unfunny. The mean reaction time was 3513.2 ms (S.D.¼177.24 ms) in the funny condition, and 3820.2 ms (S.D.¼177.24 ms) in the unfunny condition. There was no significant difference in the reaction time between the two conditions (F (1, 38)¼ 1.40, p¼0.24). We analyzed post-scan ratings on a scale from 0 to 5 (1 ¼least funny, 5¼ most funny, and the considered unfunny were given a zero). The mean ratings for the funny and unfunny conditions were as follows. The mean ratings for the funny condition was 2.29, S.D. ¼0.63 and the mean ratings for unfunny condition was 0.27, S.D. ¼0.37. A one-way ANOVA yielded significant differences between the two experimental conditions (F (1, 55) ¼420.76, po 0.0001). We also analyzed predictability of the content of the

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Table 1 Brain regions showing significant BOLD signal increases during each condition (Target sentence). Region of activation

Left/Right

Funny Inferior frontal/insula Inferior frontal/insula Inferior frontal Superior frontal Anterior cingulate Middle frontal Middle temporal Middle temporal Temporal pole Angular (TPJ) Superior temporal (TPJ) Angular (IPL) Inferior parietal Midbrain Midbrain Lentiform nucleus

L R R L R L L R L L R R L L R L

Unfunny Inferior frontal Inferior frontal Superior frontal Medial frontal Middle frontal Middle frontal Middle Temporal Inferior Parietal Thalamus Caudate

L R L R L R R L L R

Brodmann area

Voxels

45/47 44/47 46

T value

1382 576 214 1191 329 108 137 78 191 14 37 16 1003

21 38 39 22 40 40

221 45/47 44/47

827 890 996

8 9 9

106 214 53 134 28

P cluster

MNI cordinates X

Y

Z

13.59 12.63 8.29 11.77 8.58 10.01 8.00 8.61 8.80 8.79 6.86 7.24 6.87 12.80 10.30 9.63

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.008 0.001 0.006 0.000 0.000 0.000

 34 34 56 8 8  44  56 52  48  58 66 64  50 4 8  12

16 24 24 14 22 12  24  20 8  58  50  54  58  18  12 4

 14  10 32 62 46 50 6 8  22 28 10 30 46 8 4 2

13.63 11.70 12.66 9.38 8.40 9.79 13.12 8.13 8.68 7.28

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

 42 34 8 4  50 48 50  36 4 14

20 24 14 22 16 14  22  52  26 12

4  10 60 48 30 36 6 52 2 4

Brain regions showing significant BOLD signal increases of funny versus unfunny condition (Target sentence). Region of activation

Funny versus unfunnya Medial frontal(MPFC) Medial frontal (VMPFC) Inferior frontal/insula Inferior frontal Superior frontal Middle temporal Temporal pole Angular (IPL) Angular (TPJ) Anterior cingulate Hippocampus Hippocampus Amygdala Amygdala Midbrain Midbrain Lentiform nucleus

Left/Right

L L L L L R R L R L L R L R L R R

Brodmann area

9 10 47 9 21 38 40 24

Voxels

142 47 52 38 55 16 16 15 20 19 91 140 16 48 87 35 14

T value

5.26 4.32 4.47 3.65 4.10 4.46 3.82 4.11 3.08 4.03 5.24 6.84 3.98 4.57 5.34 4.17 4.12

P value (SVC corrected)

0.000 0.005 0.004 0.012 0.004 0.012 0.010 0.013 0.036 0.011 0.002 0.000 0.012 0.003 0.002 0.007 0.013

MNI coordinates X

Y

Z

 12 4  36  40  14 58 46  56 50 4  28 30  22 22 6 6 16

44 46 18 28 38 4 16  48  60 28  22  16 8 8  22  22 4

24 8  14 8 44  22  32 52 28 4  14  20  16  16 4 2 4

Activation threshold was set at Po 0.05, corrected for multiple comparisons at the cluster level for the whole brain. a

A small volume correction (SVC) with a sphere of 6-mm radius was used for the contrast of funny versus unfunny condition.

target sentence in the post-scan questionnaire. Categorical variables were compared between funny and unfunny conditions using Fisher's exact test. We found that predictability was significantly lower (18%) in the funny condition than in the unfunny condition (27%; P ¼0.0001). 3.2. Imaging results 3.2.1. Whole-brain analysis The whole-brain analysis of the imaging results produced several findings. First, the regions activated by the first two sentences were delineated (Supplementary Table S1). Specifically, when we compared the differences between the activation elicited in the funny condition

and that in the unfunny condition, we found no significant differences. We also analyzed the regions that were responsive to the third sentence (Supplementary Table S2). The imaging revealed that a small cluster in the middle frontal gyrus ( 20, 2, 46) was activated in the contrast of funny versus unfunny condition. The regions that were responsive to the third sentence were also analyzed (Supplementary Table S2). Next, to identify the regions underlying humor comprehension, we analyzed the regions responsive to the target sentence. In the funny condition, we found activation in the bilateral inferior frontal gyrus (IFG: BA 45/47), middle frontal gyrus (MFG), middle temporal gyrus (MTG: BA 21), temporo-parietal junction (TPJ: BA 22/39), inferior parietal lobule (IPL: BA 40), left superior frontal gyrus (SFG), left temporal pole (BA38). In the mesolimbic regions, we found

M. Shibata et al. / Neuropsychologia 65 (2014) 137–145

activation in the bilateral midbrain, and left lentiform nucleus. In the unfunny condition, we observed activation in the bilateral IFG (BA 45/ 47), SFG, MFG (BA 9), right MTG, left IPL (BA 40), thalamus and caudate (po0.05, FWE, Table 1) We also tested the brain activity in the contrast of funny versus unfunny condition by using after small volume correction (SVC) with a sphere of 6-mm radius. The contrast revealed greater activation in the left MPFC (BA 9), VMPFC (BA 10), IFG ( BA 47), SFG, anterior cingulate (ACC), right MTG (BA 21), bilateral IPL (BA 40; extending into TPJ) hippocampus, amygdala, midbrain, and right lentiform nucleus (Po0.05, FWE-corrected SVC, Fig. 2, Table 1).

3.2.2. Post-scan subjective funniness ratings: parametric modulation analysis A post-hoc covariate analysis examining the association between humor intensity (i.e., degree of funniness as rated by

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each participant) and the BOLD signal magnitude showed that the humor intensity was associated with increased activation in the bilateral thalamus, midbrain (substantia nigra/ventral tegmental area), and left MTG (Fig. 3, Table 2).

3.2.3. PPI analysis We used PPI analyses to investigate task-specific changes in functional connectivity between the seed regions and the other brain regions involved in humor comprehension. Within the four seed regions, the left IFG showed enhanced connectivity with the right IFG, STG, thalamus and midbrain. The left IPL showed enhanced connectivity with the left midbrain, right thalamus, STG and MTG. The right MTG showed enhanced connectivity with the bilateral thalamus, right midbrain, SFG, STG, left MTG, and caudate. The left SFG showed enhanced connectivity with the left STG, PCC, lingual gyrus and right MTG (Fig. 4 and Table 3).

Fig. 2. The activation of the contrast in the funny condition versus the unfunny condition during the target sentence. The parameter estimate graphs of the funny sentence (blue) and the unfunny sentence (red) are presented as the mean values for 20 participants. The error bars indicate the standard error of the mean. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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4. Discussion In this study, we examined the relationship between cognitive and affective components involved in humor comprehension processing. Our stimuli consisted of sentences that were nearly identical across conditions, such that any differences between conditions would be specific to the neural mechanisms involved in humor comprehension processing. Our results support our hypothesis, and demonstrate that the punch line (target sentence) in the funny condition, as compared to the last sentence in the unfunny condition, induced a perception of funniness and elicited greater activation in the language and semantic networks as well as mesolimbic reward regions.

4.1. Activation in language and semantic networks Our fMRI analysis indicated that the punch line in the funny condition, as compared with the last sentence in the unfunny condition, activated the left MPFC (BA 9), VMPFC (BA 10), IFG ( BA 47), SFG, anterior cingulate (ACC), right MTG (BA 21), bilateral IPL (BA 40; extending into TPJ) hippocampus, amygdala, midbrain, and right lentiform nucleus (Table 1). These results suggest that the right MTG, the left MPFC, IFG, SFG, and the IPL are involved in comprehension processing such as incongruity detection and semantic integration (incongruity resolution).

Fig. 3. Activated regions correlated with subjective funniness ratings. The results showed activation in the (A) thalamus, (B) midbrain (substantia nigra/ventral tegmental area), (C) ventral striatum, and (D) MTG.

We first focused on activation in the right MTG, which may be involved in detecting incongruity. Previous neuroimaging studies have reported an increased BOLD response in the MTG during the various tasks such as detection of a social signal (Sugiura et al., 2014), detection of deception (Cui et al., 2014), and joke comprehension. Goel and Dolan (2001) found increased activation in the bilateral MTG during joke comprehension, and Moran et al. (2004) found activation of the right MTG during humor detection. The results in Chan et al. (2012b) also showed that detection of incongruity was associated with greater activation in the right MTG and the right MFG by comparing the nonsensical condition with the unfunny condition. Other studies of language processing (not involving humor) have reported that the right MTG is involved in detecting semantic violations (Kuperberg et al., 2000; Newman et al., 2001; Ni et al., 2000). Thus, the right MTG may play a specific role in processes underlying verbal humor, such as incongruity detection. In the present study, we detected greater activation in the IFG, SFG, and IPL in the funny condition compared to the unfunny condition. Regarding the observed activation in the left IFG, the comprehension of a semantic joke requires pragmatic knowledge about the world, such as prejudice and social conventions (Chan et al., 2012a; Goel and Dolan, 2001). From a text-linguistic perspective, jokes use unexpected responses that initially create a pragmatic violation (perception of incongruity). Only the subsequent reinterpretation process renders the jokes coherent, and so a pragmatic violation of sentence context elicits frontal– temporal network activation that is related to lexico-semantic processing (Ferstl et al., 2008). Moreover, previous functional neuroimaging studies have reported an increased BOLD response in the IFG during various tasks: sentence and discourse comprehension (bilateral IFG) (Dapretto and Bookheimer, 1999; Kuperberg et al., 2006; Rodd et al., 2005; Zempleni et al., 2007), the detection of semantic anomalies (left IFG) (Hagoort et al., 2004; Ni et al., 2000), the presentation of an ambiguous statement (bilateral IFG) (Rodd et al., 2005; Zempleni et al., 2007), and the construction of a situation model (bilateral IFG) (Ferstl et al., 2005; Menenti et al., 2009). In light of these previous findings, one plausible explanation for the observed IFG involvement in our study is that this region plays a key role in the processing of verbal humor comprehension, such as incongruity detection and semantic integration (incongruity resolution). In addition to IFG activation, we also observed greater activation in the left SFG and IPL in the funny condition compared to the unfunny condition. Recent studies suggest that the left SFG and IPL may be associated with the humor comprehension integration process. Specifically, these regions may play a role in connecting the causal relationships between the setup and punch lines (Bekinschtein et al., 2011; Samson et al., 2009). The results in Chan et al. (2012b) also indicate that the resolution of incongruities was associated with greater activation in the left SFG and IPL when comparing the funny condition to the nonsensical condition.

Table 2 Brain regions showing activated regions covarying with degree of Humor intensity (small volume corrected). Region of activation

Funny sentence Thalamus Thalamus Midbrain Midbrain Ventral striatum Middle temporal

Left/Right

L R L R R L

Brodmann area

21

Voxels

49 7 48 12 10 24

T value

4.32 3.30 3.65 3.57 3.23 3.16

P value (SVC corrected)

0.018 0.035 0.018 0.035 0.041 0.028

MNI cordinates X

Y

Z

 22 10  12 10 20  56

 28  18  26  22  14 2

2 6 6 8 2  18

M. Shibata et al. / Neuropsychologia 65 (2014) 137–145

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Fig. 4. Results of PPI analysis. Brain areas showing enhanced connectivity with seed regions (MTG, IPL, IFG and SFG).

Table 3 PPI in each seed. Seed

Left/Right

Area

Voxels

T value

P value (SVC corrected)

MNI X

Y

Z

Left IFG

R R R R

IFG STG Thalamus Midbrain

72 82 35 15

6.73 5.18 4.33 4.07

0.002 0.001 0.004 0.007

28 44 4 6

24  32  32  12

8 2 6 2

Left IPL

L R R R

Midbrain Thalamus STG MTG

60 10 27 48

4.69 3.85 4.36 4.06

0.003 0.008 0.005 0.004

6 2 48 54

 24  26  20  30

2 0 8 4

Right MTG

R L L L R R L

Thalamus Thalamus Midbrain MTG SFG STG Caudate

59 10 36 14 34 27 11

5.11 5.02 5.02 4.22 4.08 4.03 3.77

0.002 0.008 0.004 0.007 0.005 0.005 0.008

10  12 6  66 10 50  12

 10  12  16  32 62  18 10

0 8 6 6 36 6 8

Left SFG

L L L R

STG PCC Lingual MTG

44 21 24 23

5.08 4.67 4.45 3.97

0.003 0.006 0.005 0.006

 44  24 4 46

 28  38  64 6

6 42 2  34

Note: IFG; inferior frontal gyrus, STG; superior temporal gyrus, IPL; inferior parietal lobule, MTG; middle temporal gyrus, SFG; superior frontal gyrus, PCC; posterior cingulate (small volume corrected).

Furthermore, a recent meta-analysis indicated that a region containing the IPL and extending into the temporo-occipito-parietal junction (TPJ/TOPJ; BA37, BA39 and BA40) is central to incongruity detection and resolution (Vrticka et al., 2013b). While these findings will need to be followed up using other tasks and methodologies to circumvent the reverse inference problem (Poldrack, 2011), our results suggest that these cortical networks are the main processing regions associated with incongruity detection and resolution.

4.2. Activation of the mesolimbic reward system In the present study, we found higher activation in the hippocampus, amygdala, midbrain, and right lentiform nucleus in the funny versus unfunny conditions. Moreover, a parametric modulation analysis of the subjective funniness ratings also revealed the humor intensity to be associated with increased activation in dopaminergic reward regions. These findings indicate that the dopaminergic reward system is involved in coding funniness and eliciting

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associated feelings of amusement. Recent neuroimaging studies have indicated that both the lentiform nucleus and the midbrain are implicated in positive reward prediction errors (D’Ardenne et al., 2008; O’Doherty et al., 2006), as well as self-reported happiness and monetary rewards (Knutson and Cooper, 2005; Knutson et al., 2001) and are activated during the detection of attractive faces (Cloutier et al., 2008) and in addiction (Reuter et al., 2005). Studies regarding humor comprehension have indicated that subcortical regions, including the amygdala, nucleus accumbens, midbrain (VTA), and hypothalamus, contribute to the aspect of humor appreciation (Franklin and Adams, 2011; Azim et al., 2005; Mobbs et al., 2003, 2005; Moran et al., 2004; Schwartz et al., 2008; Vrticka et al., 2013a). In the present experiment, we assessed the predictability of the content of the target sentence. We found that in the funny condition, predictability was significantly lower than that in the unfunny condition. This suggests that in the funny condition, the participants did not expect (did not predict) the punch line based on the prior context. Consequently, they might have been surprised when the punch line arrived. Such unexpected stimuli may have induced activity in dopaminergic reward regions, resulting in a reward prediction error. Thus, increased activation in the dopaminergic reward regions, as well a correlation between humor intensity (i.e., degree of funniness as rated by each participant) may reflect positive reward prediction errors. Moreover, a funny versus unfunny contrast revealed higher activation in the amygdala. Previous neuroimaging studies have reported amygdala activations during humor appreciation (Bekinschtein et al., 2011; Chan et al., 2012a, 2012b; Kohn et al., 2011; Mobbs et al., 2003, 2005; Moran et al., 2004; Vrticka et al., 2013c). Additionally, the amygdala has been found to contribute to positive emotion and reward (Murray, 2007), and to play a key role in information processing including processing of salience, significance, ambiguity, and unpredictability (Pessoa and Adolphs, 2010). That the amygdala is active during humor appreciation may reflect the role of this region in processing positive emotions and unpredictable information. 4.3. How do the cognitive components elicit the affective components of humor appreciation? Another purpose of this study was to investigate the functional connectivity between the regions involved in cognitive affective interaction of humor comprehension using PPI analysis. First, our results revealed that language and semantic regions, such as the IFG, MTG, STG, SFG and IPL, are simultaneously co-activated during humor comprehension processing. Our results also revealed the network involved in the cognitive processing, such as incongruity detection and incongruity resolution processes. Second, PPI analysis revealed that the MTG, IPL and IFG showed enhanced connectivity with the midbrain during humor comprehension processing. Our results suggested that these regions involved in the cognitive processes were co-activated with the midbrain which is involved in the affective processes. Based on the two-stage and three-stage models of humor comprehension, Chan et al. (2012b) proposed a step-by-step process for humor comprehension. The comprehension of verbal humor starts with the processing of semantic meaning and the identification of incongruities in the right MTG and right MFG. This process is followed by semantic selection and integration associated with resolution of these incongruities in the bilateral IFG, left SFG and left IPL. Finally, the left VMPFC, right ACC and the subcortical bilateral amygdalae and bilateral parahippocampal gyri appear to be responsible for the affective response to humor during the elaboration stage. However, due to the temporal resolution problems associated with fMRI, it is difficult to temporally dissociate these comprehension processes. Moreover, recent studies suggest that cognitive and affective processes

intersect and interact in the language and semantic regions, as well as the dopaminergic reward regions, thereby influencing one another reciprocally (Cole et al., 2012). Our findings from the PPI analysis may reflect the interaction of these pathways in humor comprehension. 4.4. Limitations There are some limitations to our findings. Our study focused on verbal humor processing. However, the various elements are involved in humor comprehension processing. Previous studies have examined these elements from various angles (e.g., incongruityresolution and nonsense cartoons: Samson et al., 2009; humorous and nonhumorous insight: Amir et al., 2013; comparison between Funny and Positive (enjoyable but not funny) stimuli: Neely et al., 2012). Different approaches are required to elucidate the respective brain regions involved in these elements. Another limitation of this study relates to the temporal processes associated with humor comprehension. According to the incongruity-resolution model or three-stage model of humor comprehension (Chan et al., 2012b), humor comprehension starts with the processing of semantic meaning and the identification of incongruities. This process is followed by semantic selection and integration associated with the resolution of these incongruities. Because of temporal resolution problems associated with fMRI, these processes have not been functionally and anatomically dissociated. Further research on temporal processes is needed to clarify these mechanisms. 5. Conclusion We examined the relationship between these cognitive and affective components of humor comprehension using fMRI. Our results indicate that the punch line (target sentence) in the funny condition induced a perception of funniness and caused a greater activation in language and semantic regions, as well as in mesolimbic reward regions. Our results confirm that the network including the right MTG, the left IPL, the IFG and the mesolimbic region plays a critical role in the interaction between cognitive and affective components of humor appreciation. These results suggest that interconnectivity among these regions integrates the cognitive and affective components of humor to elicits positive emotional responses.

Acknowledgments This work was supported by the Japan Society for the Promotion of Science (Grant number, 22500239) and the Global COE Program “Centre for Advanced Research on Logic and Sensibility” by the Ministry of Education, Culture, Sports, Science, and Technology (MEXT), Japan. We are grateful to everyone who participated in our study.

Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.neuropsychologia. 2014.10.025. References Amir, O., Biederman, I., Wang, Z., Xu, X., 2013. Ha Ha! versus Aha! A direct comparison of humor to nonhumorous insight for determining the neural correlates of mirth. Cereb. Cortex, http://dx.doi.org/10.1093/cercor/bht343. Azim, E., Mobbs, D., Jo, B., Menon, V., Reiss, A.L., 2005. Sex differences in brain activation elicited by humor. Proc. Natl. Acad. Sci. USA 102 (45), 496–501. http: //dx.doi.org/10.1073/pnas.0408456102.

M. Shibata et al. / Neuropsychologia 65 (2014) 137–145

Bekinschtein, T.A., Davis, M.H., Rodd, J.M., Owen, A.M., 2011. Why clowns taste funny: the relationship between humor and semantic ambiguity. J. Neurosci. 31 (26), 9665–9671. http://dx.doi.org/10.1523/JNEUROSCI.5058-10.2011. Biederman, I., Vessel, E.A., 2006. Perceptual pleasure and the brain. Am. Sci. 94 (3), 247. Chan, Y.C., Chou, T.L., Chen, H.C., Liang, K.C., 2012a. Segregating the comprehension and elaboration processing of verbal jokes: an fMRI study. NeuroImage 61 (4), 899–906. http://dx.doi.org/10.1016/j.neuroimage.2012.03.052. Chan, Y.C., Chou, T.L., Chen, H.C., Yeh, Y.C., Lavallee, J.P., Liang, K.C., et al., 2012b. Towards a neural circuit model of verbal humor processing: an fMRI study of the neural substrates of incongruity detection and resolution. NeuroImage 66C, 169–176. http://dx.doi.org/10.1016/j.neuroimage.2012.10.019. Cloutier, J., Heatherton, T.F., Whalen, P.J., Kelley, W.M., 2008. Are attractive people rewarding? Sex differences in the neural substrates of facial attractiveness. J. Cogn. Neurosci. 20 (6), 941–951. http://dx.doi.org/10.1162/jocn.2008.20062. Cole, D.M., Beckmann, C.F., Searle, G.E., Plisson, C., Tziortzi, A.C., Nichols, T.E., Gunn, R.N., Matthews, P.M., Rabiner, E.A., Beaver, J.D., 2012. Orbitofrontal connectivitywith resting-state networks is associated with midbrain dopamine D3 receptoravailability. Cereb. Cortex 22, 2784–2793. http://dx.doi.org/10.1093/ cercor/bhr354. 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. http://dx. doi.org/10.1016/S0304-3940(01)02387-4. Cui, Q., Vanman, E.J., Wei, D., Yang, W., Jia, L., Zhang, Q., 2014. Detection of deception based on fMRI activation patterns underlying the production of a deceptive response and receiving feedback about the success of the deception after a mock murder crime. Soc. Cogn. and Affect. Neurosci 9 (10), 1472–1480. http://dx.doi.org/10.1093/scan/nst134. Dapretto, M., Bookheimer, S.Y., 1999. Form and content: dissociating syntax and semantics in sentence comprehension. Neuron 24 (2), 427–432. http://dx.doi. org/10.1016/S0896-6273(00)80855-7. D’Ardenne, K., McClure, S.M., Nystrom, L.E., Cohen, J.D., 2008. BOLD responses reflecting dopaminergic signals in the human ventral tegmental area. Science 319 (5867), 1264–1267. http://dx.doi.org/10.1126/science.1150605. Ferstl, E.C., Rinck, M., von Cramon, D.Y., 2005. Emotional and temporal aspects of situation model processing during text comprehension: an event-related fMRI study. J. Cogn. Neurosci. 17 (5), 724–739. http://dx.doi.org/10.1162/ 0898929053747658. Ferstl, E.C., Neumann, J., Bogler, C., von Cramon, D.Y., 2008. The extended language network: a meta-analysis of neuroimaging studies on text comprehension. Hum. Brain Mapp. 29 (5), 581–593. http://dx.doi.org/10.1002/hbm.20422. Franklin Jr., R.G., Adams Jr., R.B., 2011. The reward of a good joke: neural correlates of viewing dynamic displays of stand-up comedy. Cogn. Affect. Behav. Neurosci. 11, 508–515. http://dx.doi.org/10.3758/s13415-011-0049-7. Friston, K.J., Buechel, C., Fink, G.R., Morris, J., Rolls, E., Dolan, R.J., 1997. Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6, 218–229. http://dx.doi.org/10.1006/nimg.1997.0291. Goel, V., Dolan, R.J., 2001. The functional anatomy of humor: segregating cognitive and affective components. Nat. Neurosci. 4 (3), 237–238. http://dx.doi.org/ 10.1038/85076. Goel, V., Dolan, R.J., 2007. Social regulation of affective experience of humor. J. Cogn. Neurosci. 19 (9), 1574–1580. http://dx.doi.org/10.1162/jocn.2007.19.9.1574. Hagoort, P., Hald, L., Bastiaansen, M., Petersson, K.M., 2004. Integration of word meaning and world knowledge in language comprehension. Science 304 (5669), 438–441. http://dx.doi.org/10.1126/science.1095455. Knutson, B., Cooper, J.C., 2005. Functional magnetic resonance imaging of reward prediction. Curr. Opin. Neurol. 18 (4), 411–417. Knutson, B., Fong, G.W., Adams, C.M., Varner, J.L., Hommer, D., 2001. Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport 12 (17), 3683–3687. Kohn, N., Kellermann, T., Gur, R.C., Schneider, F., Habel, U., 2011. Gender differences in the neural correlates of humor processing:implications for different processing modes. Neuropsychologia 49 (5), 888–897. http://dx.doi.org/10.1016/j. neuropsychologia.2011.02.010. Kuperberg, G.R., McGuire, P.K., Bullmore, E.T., Brammer, M.J., Rabe-Hesketh, S., Wright, I.C., et al., 2000. Common and distinct neural substrates for pragmatic, semantic, and syntactic processing of spoken sentences: an fMRI study. J. Cogn. Neurosci. 12, 321–341. http://dx.doi.org/10.1162/089892900562138. Kuperberg, G.R., Lakshmanan, B.M., Caplan, D.N., Holcomb, P.J., 2006. Making sense of discourse: an fMRI study of causal inferencing across sentences. NeuroImage 33 (1), 343–361. http://dx.doi.org/10.1016/j.neuroimage.2006.06.001. Marinkovic, K., Baldwin, S., Courtney, M.G., Witzel, T., Dale, A.M., Halgren, E., 2011. Right hemisphere has the last laugh: neural dynamics of joke appreciation. Cogn. Affect. Behav. Neurosci. 11, 113–130. http://dx.doi.org/10.3758/s13415-010-0017-7. Martin, R.A., 2007. The Psychology of Humor: An Integrative ApproachElsevier Academic Press, Burlington, MA. Menenti, L., Petersson, K.M., Scheeringa, R., Hagoort, P., 2009. When elephants fly: differential sensitivity of right and left inferior frontal gyri to discourse and world knowledge. J. Cogn. Neurosci. 21 (12), 2358–2368. http://dx.doi.org/ 10.1162/jocn.2008.21163. Mobbs, D., Greicius, M.D., Abdel-Azim, E., Menon, V., Reiss, A.L., 2003. Humor modulates the mesolimbic reward centers. Neuron 40 (5), 1041–1048. http: //dx.doi.org/10.1016/s0896-6273(03)00751-7. Mobbs, D., Hagan, C.C., Azim, E., Menon, V., Reiss, A.L., 2005. Personality predicts activity in reward and emotional regions associated with humor. Proc. Natl. Acad. Sci. USA 102 (45), 16502–16506. http://dx.doi.org/10.1073/pnas.040845 7102.

145

Moran, J.M., Wig, G.S., Adams Jr., R.B., Janata, P., Kelley, W.M., 2004. Neural correlates of humor detection and appreciation. NeuroImage 21 (3), 1055–1060. http://dx.doi.org/10.1016/j.neuroimage.2003.10.017. Murray, E.A., 2007. The amygdala, reward and emotion. Trends Cogn. Sci. 11, 489–497. http://dx.doi.org/10.1016/j.tics.2007.08.013. Neely, M.N., Walter, E., Black, J.M., Reiss, A.L., 2012. Neural correlates of humor detection and appreciation in children. J. Neurosci. 32 (5), 1784–1790. Newman, A.J., Pancheva, R., Ozawa, K., Neville, H.J., Ullman, M.T., 2001. An eventrelated fMRI study of syntactic and semantic violations. J. Psycholinguist Res. 30 (3), 339–364. http://dx.doi.org/10.1023/A:1010499119393. Ni, W., Constable, R.T., Mencl, W.E., Pugh, K.R., Fulbright, R.K., Shaywitz, S.E., et al., 2000. An event-related neuroimaging study distinguishing form and content in sentence processing. J. Cogn. Neurosci. 12 (1), 120–133. http://dx.doi.org/ 10.1162/08989290051137648. Nouchi, R., 2004. Dictionary of Joke, Humor and Esprit. Kokusho-kankoukai, Tokyo. O’Doherty, J.P., Buchanan, T.W., Seymour, B., Dolan, R.J., 2006. Predictive neural coding of reward preference involves dissociable responses in human ventral midbrain and ventral striatum. Neuron 49 (1), 157–166. http://dx.doi.org/ 10.1016/j.neuron.2005.11.014. O’Reilly, J.X., Woolrich, M.W., Behrens, T.E., Smith, S.M., Johansen-Berg, H., 2012. Tools of the trade: psychophysiological interactions and functional connectivity. Soc. Cogn. Affect. Neurosci. 7, 604–609. http://dx.doi.org/10.1093/scan/nss055. Panksepp, J., 1993. Neurochemical control of moods and emotions: amino acids to neuropeptides. In: Lewis, M., Haviland, M. (Eds.), Handbook of Emotions. Guilford Press, New York, NY, US, pp. 87–107. Papousek, I., Reiser, E.M., Weiss, E.M., Fink, A., Samson, A.C., Lackner, H.K., Schulter, G., 2013. State-dependent changes of prefrontal-posterior coupling in the context of affective processing: susceptibility to humor. Cogn. Affect. Behav. Neurosci. 13, 252–261. http://dx.doi.org/10.3758/s13415-012-0135-5. Pessoa, L., Adolphs, R., 2010. Emotion processing and the amygdala: from a ‘low road’ to ‘many roads’ of evaluating biological significance. Nat. Rev. Neurosci. 11, 773–782. Poldrack, R.A., 2011. Inferring mental States from neuroimaging data: from reverse inference to large-scale decoding. Neuron 72, 692–697. http://dx.doi.org/ 10.1016/j.neuron.2011.11.001. Rapp, A.M., Wild, B., Erb, M., Rodden, F.A., Ruch, W., Grodd, W., 2008. Trait cheerfulness modulates BOLD response in lateral cortical but not limbic brain areas–a pilot fMRI study. Neurosci. Lett. 445 (3), 242–245. http://dx.doi.org/ 10.1016/j.neulet.2008.09.017. Reuter, J., Raedler, T., Rose, M., Hand, I., Glascher, J., Buchel, C., 2005. Pathological gambling is linked to reduced activation of the mesolimbic reward system. Nat. Neurosci. 8 (2), 147–148. http://dx.doi.org/10.1038/nn1378. Rodd, J.M., Davis, M.H., Johnsrude, I.S., 2005. The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. Cereb. Cortex 15 (8), 1261–1269. http://dx.doi.org/10.1093/cercor/bhi009. Samson, A.C., Zysset, S., Huber, O., 2008. Cognitive humor processing: different logical mechanisms in nonverbal cartoons – an fMRI study. Soc. Neurosci. 3 (2), 125–140. http://dx.doi.org/10.1080/17470910701745858. Samson, A.C., Hempelmann, C.F., Huber, O., Zysset, S., 2009. Neural substrates of incongruity-resolution and nonsense humor. Neuropsychologia 47 (4), 1023–1033. http://dx.doi.org/10.1016/j.neuropsychologia.2008.10.028. Schwartz, S., Ponz, A., Poryazova, R., Werth, E., Boesiger, P., Khatami, R., et al., 2008. Abnormal activity in hypothalamus and amygdala during humour processing in human narcolepsy with cataplexy. Brain 131 (Pt 2), 514–522. http://dx.doi.org/ 10.1093/brain/awm292. Shultz, T.R., 1976. A cognitive-developmental analysis of humour. In: Chapman, A.J., Foot, H.C. (Eds.), Humour and Laughter: Theory, Research, and Applications. John Wiley, London. Sugiura, M., Yomogida, Y., Mano, Y., Sassa, Y., Kambara, T., Sekiguchi, A., Kawashima, R., 2014. From social-signal detection to higher social cognition: an fMRI approach. Soc. Cogn. Affect. Neurosci. 9 (9), 1303–1309. http://dx.doi.org/10.1093/scan/nst119. Suls, J.M., 1972. A two-stage model for the appreciation of jokes and cartoons: An information processing analysis. In: Goldstein, J.H., McGhee, P.E. (Eds.), The Psychology of Humor: Theoretical Perspectives and Empirical Issues. Academic Press, New York, pp. 81–100. Vrticka, P., Black, J., Neely, M., Walter-Shelly, E., Reiss, A., 2013a. Humor processing in children: influence of temperament age and IQ. Neuropsychologia 51 (13), 2799–2811. http://dx.doi.org/10.1016/j.neuropsychologia.2013.09.028. Vrticka, P., Black, J., Reiss, A., 2013b. The neural basis of humour processing. Nat. Rev. Neurosci. 14, 860–868. http://dx.doi.org/10.1038/nrn3566. Vrticka, P., Neely, M., Walter-Shelly, E., Black, J., Reiss, A., 2013c. Sex-differences during humor appreciation in child-sibling pairs. Soc. Neurosci. 8 (4), 291–304. http://dx.doi.org/10.1080/17470919.2013.794751. Watson, K.K., Matthews, B.J., Allman, J.M., 2007. Brain activation during sight gags and language-dependent humor. Cereb. Cortex 17 (2), 314–324. http://dx.doi. org/10.1093/cercor/bhj149. Wild, B., Rodden, F.A., Rapp, A., Erb, M., Grodd, W., Ruch, W., 2006. Humor and smiling: cortical regions selective for cognitive, affective, and volitional components. Neurology 66 (6), 887–893. http://dx.doi.org/10.1212/01. wnl.0000203123.68747.02. Zempleni, M.Z., Renken, R., Hoeks, J.C., Hoogduin, J.M., Stowe, L.A., 2007. Semantic ambiguity processing in sentence context: evidence from event-related fMRI. NeuroImage 34 (3), 1270–1279. http://dx.doi.org/10.1016/j.neuroimage.2006. 09.048. Zempleni, M.Z., Haverkort, M., Renken, R., Stowe, L.A., 2007. Evidence for bilateral involvement in idiom comprehension: an fMRI study. NeuroImage 34 (3), 1280–1291. http://dx.doi.org/10.1016/j.neuroimage.2006.09.049.