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Abstract

Background: The interrelationships among humor, smiling, and grinning have fascinated philosophers for millennia and neurologists for over a century. A functional dissociation between emotional facial expressions and those under voluntary control was suggested decades ago. Recent functional imaging studies, however, have been somewhat at odds with older studies with respect to the role of the right frontal cortex in the perception of humor.

Methods: Blood oxygen level–dependent (BOLD) activity was measured in 13 subjects during the presentation of “funny” vs “nonfunny” versions of essentially the same cartoons and compared with BOLD activity associated with “merely grinning” at similar nonfunny cartoons via fMRI.

Results: Humor perception was correlated with BOLD activity in the left temporo-occipitoparietal junction and left prefrontal cortex and humor-associated smiling (recorded with an MR-compatible video camera) with bilateral activity in the basal temporal lobes. Unexpectedly, both conditions were also accompanied by a decrease in BOLD activity in the right orbitofrontal cortex. Voluntary “grinning” in the absence of humorous stimuli was accompanied by bilateral activity in the facial motor regions.

Conclusions: These results confirm the clinically derived hypothesis of separate cortical regions responsible for the production of emotionally driven vs voluntary facial expressions. The right orbitofrontal decrease reconciles inconsistencies between clinical and functional imaging findings and may reflect a disinhibition of facial emotional expression.