Abstract
Humor processing involves distinct processing stages including incongruity detection, emotional response, and engagement of mesolimbic reward regions. Dysfunctional reward processing and clinical symptoms in response to humor have been previously described in both hypocretin deficient narcolepsy-cataplexy (NC) and in idiopathic Parkinson disease (PD). For NC patients, humor is the strongest trigger for cataplexy, a transient loss of muscle tone, whereas dopamine-deficient PD-patients show blunted emotional responses to humor. To better understand the role of reward system and the various contributions of hypocretinergic and dopaminergic mechanisms to different stages of humor processing we examined the electrophysiological response to humorous and neutral pictures when given as reward feedback in PD, NC and healthy controls. Humor compared to neutral feedback demonstrated modulation of early ERP amplitudes likely corresponding to visual processing stages, with no group differences. At 270 ms post-feedback, conditions showed topographical and amplitudinal differences for frontal and left posterior electrodes, in that humor feedback was absent in PD patients but increased in NC patients. We suggest that this effect relates to a relatively early affective response, reminiscent of increased amygdala response reported in NC patients. Later ERP differences, corresponding to the late positive potential, revealed a lack of sustained activation in PD, likely due to altered dopamine regulation in reward structures in these patients. This research provides new insights into the temporal dynamics and underlying mechanisms of humor detection and appreciation in health and disease.
Highlights
Research in the field of humor processing has taken several key steps over the past two decades, both in terms of its underlying neurobiology and its psychological functions [1,2]
Neuroimaging studies have largely focused on the spatial characteristics of humor processing using functional magnetic resonance imaging, while few studies have examined the temporal dynamics of these processes using magneto/electroencephalography (MEG/EEG)
This study focused on participant’s active manipulation of the late positive potential (LPP), which has been linked to the underlying activity in reward related structures [10,11]
Summary
Research in the field of humor processing has taken several key steps over the past two decades, both in terms of its underlying neurobiology and its psychological functions [1,2]. Two major dimensions of humor processing have been left relatively unexplored to date. Neuroimaging studies have largely focused on the spatial characteristics of humor processing using functional magnetic resonance imaging (fMRI; [3,4,5]), while few studies have examined the temporal dynamics of these processes using magneto/electroencephalography (MEG/EEG). EEG and MEG studies to date have focused almost exclusively on the dynamics of verbal humor comprehension; with a particular focus on the so-called N400 component [6,7,8]. Many fMRI studies found that regions implicated in humor appreciation and experiencing positive rewards are largely overlapping and include dopaminergic regions of the midbrain and ventral striatum, as well as the amygdala [3,4,5], yet no study has used humorous stimuli as a specific reward signal
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