We investigated neural activation underlying humor specifically as it applies to a naturalistic, dynamic social interaction, to address the puzzling lack of evidence for mesolimbic responses using such dynamic stimuli. The present study examined the neural activation associated with watching stand-up comedians, specifically contrasting high- and low-amusing skits of the same comedians, as selected based on preratings made by a sample of raters from the same student population. Although stand-up comedy is certainly still a performance art, it simulates the joke-telling experience in everyday life, where one person surrounded by others captures the attention of the group and delivers the necessary cognitive structure and elements to produce a mirth response and receive the social capital that comes with it.
To our knowledge, the only other study that has used dynamic stimuli reported no evidence for activation in reward centers (Moran et al., 2004). However, in the present work we found activation of reward centers when contrasting high versus low humor using highly controlled and ecologically valid stimuli. In this case, we used a comparison that more closely matched that employed in studies examining cartoon humor, thereby helping reconcile the apparent discrepancy of the previous findings. This finding demonstrates that dynamic displays of social humor do appear to activate reward centers. We also found activation in several brain regions that have been more consistently implicated in understanding and experiencing humor. These include the inferior frontal cortex and temporoparietal junction (TPJ). Both of these regions have been previously shown to be involved in the detection of humor (Mobbs et al., 2003; Moran et al., 2004). The inferior frontal cortex and TPJ are both considered to be involved with decoding others’ mental states (e.g., Frith & Frith, 1999), which is important for understanding humor. This is especially important in understanding how a joke’s punch line often resolves incongruities between the mental state of a subject in a joke and the mental state of the audience of a joke (Bartolo et al., 2006), which may reflect why these regions are active here. The social nature of the present task highlights this possibility. However, it is also possible that these regions could be involved in humor appreciation for other reasons, including the roles of the inferior frontal cortex and TPJ in attentional switching. Both of these regions are active when disengaging from invalid visual cues (e.g., Arrington, Carr, Mayer, & Rao, 2000), and activity here may reflect the importance in disengaging from mental operations involved with incongruities that are linked to humor.
We also examined a regression using the fMRI participants’ own ratings of humor. Although this analysis lacks the control of our direct comparison, it also more precisely reflects participants’ own subjective experiences while in the magnet. This analysis revealed many of the same regions active as found in the direct contrast of prerated high versus low humor, including the mesolimbic reward regions including the left putamen, as well as regions involved in mental state decoding such as the TPJ. Additionally, we found activation in other regions that were not active for the clips prerated as high versus low in humor. These regions also included reward regions such as bilateral caudate and putamen, as well as the amygdala. Additional regions involved in mental state inference were active for this contrast as well, including the temporal poles and STS. Both of these regions are known to be involved with deciphering what others are thinking, with the STS specifically involved with decoding information important to the intent of others, such as biological motion, facial emotion, and eye gaze, while the temporal poles are implicated in recalling socially relevant memory, such as social scripts (Allison, Puce, & McCarthy, 2000; Gallagher & Frith, 2003). The parahippocampal cortex was also active, replicating previous similar findings (e.g., Moran et al., 2004; Watson et al., 2007), which might be due to memory of social scripts that are then violated as part of the expectancy violation model of humor.
We also found activation reflecting a negative association between humor experience ratings and the insula, posterior cingulate, and vmPFC. This seems surprising, given that the vmPFC is known to be involved in decoding humor (e.g., Goel & Dolan, 2001) via understanding others’ mental states (e.g., Mitchell, Banaji, & Macrae, 2005). It is possible that activation in the vmPFC may reflect greater attempts to understand the humor in the clips rated as less amusing. Additionally, the posterior cingulate, insula, and vmPFC are also regions implicated as part of the default network of the brain, a network involved in stimulus-independent thought and frequently active in rest periods of fMRI experiments (Buckner, Andrews-Hanna, & Schacter, 2008). Indeed, activity in each of these three regions has been positively correlated with the amount to which participants’ minds wander during an fMRI experiment (Mason et al., 2007). Thus, activation in these regions for this contrast may simply reflect participants’ reduced engagement in the task while watching low-humor clips.
Humor studies have found inconsistent results for eliciting reward activation. One possible explanation is that studies finding reward activation, including the present study, have emphasized the affective response or the feeling involved with humor. Other studies, focusing more on the quality of humor, have failed to find reward activity, presumably because of the focus on more cognitive aspects of humor (e.g., Bartolo et al., 2006). However, this difference does not explain all studies that have not reported reward-related activation. For instance, Moran et al. (2004) had participants passively view a sitcom and examined humor responses locked to a laugh track. Participants’ humor responses were thus measured in the context of an ongoing humorous episode, where humor was anticipated at any moment in the episode. This consistent anticipated reward might have led to mesolimbic activation in other portions of the episode, which thus would have been subtracted out of any direct comparison. Therefore, the high level of control offered between high and low humor, as well as the sensitivity offered by examining participants’ own ratings, may have been key to our finding mesolimbic activation in the present study. What is clear in the present study is that funnier dynamic joke-telling yielded greater activation in the reward network, as expected, and as previously found when examining cartoon humor using a similarly controlled paradigm. These findings, therefore, offer further evidence consistent with current theories that critically hinge on the presumption that reward responses are fundamental to the humor process (e.g., Hurley et al., 2011).
Interestingly, this work seems to indicate that the social humor we find funniest also involves activation of brain regions required to process social intent. Several humor studies using static cartoons have found activation in brain regions involved with decoding what others are thinking, such as the temporal poles, TPJ, and STS (e.g., Azim et al., 2005; Goel & Dolan, 2001; Mobbs, Hagan, Azim, Menon, & Reiss, 2005). These areas are more active for cartoons that involve taking others’ perspectives into account (e.g., Samson, Zysset, & Huber, 2008), a finding that highlights their importance in incorporating knowledge of others’ mental states in humor. The study here, using dynamic displays of humor, revealed that brain regions involved with decoding the social intent of others are related to greater humor experience, perhaps reflecting the processing of incongruity between social actions and expectations.
This study builds upon Moran et al.’s (2004) findings by indicating that more naturalistic humor is indeed perceived and processed as a rewarding stimulus. We enjoy humor from others, and humor plays a role in how we judge them (Wanzer et al., 1996). This may be because we find humor rewarding and associate that reward with those who produce it. This may help address why humor is generally regarded as an important social skill. A parallel may be drawn with perceived attractiveness. Physical attractiveness in others activates many of the same reward brain regions as humor (Aharon et al., 2001; O’Doherty et al., 2003), and attractiveness is likewise associated with positive halo effects and increased liking (e.g., Dion, Berscheid, & Walster, 1972). Likewise, reward activation associated with humor may contribute to why we like those who are funny, though this remains an empirical question that warrants future research.
In sum, this article reveals that ecologically relevant, dynamic displays of humor do elicit reward-related activation in the brain. This extends prior research of this kind by showing that more socially relevant forms of humor induce brain activation in much the same way as cartoons do when subjected to similar experimental controls, and it may offer insight as to why humor is so critical a social skill.