Trait cheerfulness modulates BOLD response in lateral cortical but not limbic brain areas—A pilot fMRI study

Abstract

Having a good "sense of humor" is an important personality characteristic that significantly influences social communication and may represent an important coping strategy. To take things "with humor" does not only represent a state characteristic but also a personality trait that can reliably be assessed with questionnaires like the "state-trait-cheerfulness-inventory" (STCI) by Ruch [Ruch et al., Assessing the "humorous temperament": construction of the facet and standard trait forms of the statetrait-cheerfulness-inventory-STCI, Humor 9 (1996) 303-339]. Substantial inter-individual differences among study subjects are a key feature of almost all functional magnetic resonance imaging studies on higher cognitive functions. Usually, they are considered as "statistical noise" and are not recommended for the data analysis, although they can have a high intra-individual stability. However, a number of recent fMRI studies found robust correlations between inter-individual differences in BOLD response and personality traits such as extraversion. The aim of this pilot exploratory study was to localise regions where the BOLD response was predicted by "humor personality" scores. 10 healthy male subjects viewed funny or non-funny versions of Gary Larson cartoons while BOLD response was measured with functional magnetic resonance imaging (fMRI). Data were collected from the whole brain (28 slices, slice thickness 4 mm, 1 mm gap, TR = 3 s). SPM 99 software was used. A simple regression analysis with the sub-score cheerfulness from the STCI was applied. Higher cheerfulness in the STCI predicted brain activation in the right inferior parietal lobule (Tal X, Y, Z: 45, −77, 29), but not in limbic and prefrontal brain areas. We conclude that neural correlates of cheerfulness are correlated with BOLD response in lateral cortical rather than limbic brain areas. Likely the activated region is important for a readiness or tendency to be amused, whereas the regions previously shown to be activated in humor appreciation studies are related to the understanding of the joke and the emotional reaction. Having a good "sense of humor" is an important personality characteristic that significantly influences social communication and may represent an important coping strategy. To take things "with humor" does not only represent a state characteristic but also a personality trait that can reliably be assessed with questionaires like the "state-trait-cheerfulness-inventory" (STCI-T) by Ruch (Ruch et. al., Humor 9 (1996) 303-339).Substantial inter-individual differences among study subjects are a key feature of almost all functional magnetic resonance imaging studies on higher cognitive functions. Usually, they are considered as "statistical noise" and are not recommended for the data analysis, although they can have a high intra-individual stability. However, a number of recent fMRI studies found robust correlations between inter-individual differences in BOLD-response and personality traits such as extraversion.The aim of this ...

Rostral anterior cingulate activity generates posterior versus anterior theta activity linked to agentic extraversion

“…Eisenberger et al (2005) observed a positive correlation in a more rostral ACC locus during an oddball paradigm, which is less demanding than are three-back working memory tasks. Using emotional-motivational tasks (e.g., emotional Stroop, emotion induction), most studies showed a positive correlation (e.g., Canli et al, 2004;Canli et al, 2001;Haas et al, 2006;Keightley et al, 2003; for a negative correlation, see Fruehholz et al, 2010;Rapp et al, 2008). During resting state, positive (e.g., Ebmeier et al, 1994;Sugiura et al, 2000), as well as negative (e.g., Hermes, 2007), associations were detected.…”

“…c Approximating and projecting peak activations (x-coordinates for all peaks within X ± 1 cm) from prior positron emission tomography (PET; Johnson et al, 1999;Keightley et al, 2003), single photon emission computed tomography (SPECT; Sugiura et al, 2000), continuous arterial spin labeling (CASL; Hermes, 2007), and functional magnetic resonance imaging studies (fMRI; Canli et al, 2004;Canli et al, 2001;Eisenberger et al 2005;Fruehholz et al 2010;Gray & Braver, 2002;J. R. Gray et al, 2005;Haas et al, 2006;Kumari et al, 2004;Rapp et al, 2008) investigating extraversion effects under resting conditions (circles), while emotional/motivational tasks (triangles) and cognitive tasks (squares) were performed, on the sagittal slice of the present LORETA solution running through the BA 24 peak voxel (MNI-coordinates x = 4, y = 31, z = 22). For all studies, sample size, the extraversion scale employed, and the direction of the extraversion-ACC relation (+ = positive correlation; -= negative correlation) are provided.…”

“…Various findings highlight the importance of the reward system's sensitivity (and its positive emotional impact) for individual differences in extraversion under emotional/ motivational stimulus processing (e.g., Barros-Loscertales et al, 2010;Beaver et al, 2006;Cohen, Young, Baek, Kessler, & Ranganath, 2005). Especially the ACC, as one of the major targets of reward-related midbrain dopamine projections (Allman, Hakeem, Erwin, Nimchinsky, & Hof, 2001), appears to be a central structure of the reward circuit related to extraversion and related traits in a variety of experimental settings, ranging from resting condition (e.g., Ebmeier et al, 1994;Hermes, 2007;Johnson et al, 1999;Sugiura et al, 2000) to emotional/motivational (e.g., Canli, Amin, Haas, Omura, & Constable, 2004;Canli et al, 2001;Eisenberger, Lieberman, & Satpute, 2005;Fruehholz, Prinz, & Herrmann, 2010;Haas, Omura, Amin, Constable, & Canli, 2006;Hermes, 2007;Keightley et al, 2003;Rapp et al, 2008) and cognitive (e.g., Gray & Braver, 2002;Gray et al, 2005;Kumari, ffytche, Williams, & Gray, 2004) tasks. Recent research on the neurobiology of major depression has also focused on the ACC.…”

Integration of cognitive and affective networks in humor comprehension

“…Over the past decade, many neuroimaging studies have examined the neural substrates involved in humor comprehension (Bekinschtein et al, 2011;Chan et al, 2012aChan et al, , 2012bFranklin and Adams, 2011;Dolan, 2001, 2007;Marinkovic et al, 2011;Mobbs et al, 2003Mobbs et al, , 2005Moran et al, 2004;Neely et al, 2012;Rapp et al, 2008;Samson et al, 2009Samson et al, , 2008Vrticka et al, 2013aVrticka et al, , 2013cWatson 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.…”

State-dependent changes of prefrontal–posterior coupling in the context of affective processing: Susceptibility to humor

“…It seems more likely, therefore, that the greater importance of right-than left-hemisphere prefrontal-posterior (de-)coupling in the present results is related to the processing of social-emotional information rather than to cognitive processes implicated in the perception of humor (cf. Rapp et al, 2008).…”