Abstract
Laughter is an ancient signal of social communication among humans and non-human primates. Laughter types with complex social functions (e.g., taunt and joy) presumably evolved from the unequivocal and reflex-like social bonding signal of tickling laughter already present in non-human primates. Here, we investigated the modulations of cerebral connectivity associated with different laughter types as well as the effects of attention shifts between implicit and explicit processing of social information conveyed by laughter using functional magnetic resonance imaging (fMRI). Complex social laughter types and tickling laughter were found to modulate connectivity in two distinguishable but partially overlapping parts of the laughter perception network irrespective of task instructions. Connectivity changes, presumably related to the higher acoustic complexity of tickling laughter, occurred between areas in the prefrontal cortex and the auditory association cortex, potentially reflecting higher demands on acoustic analysis associated with increased information load on auditory attention, working memory, evaluation and response selection processes. In contrast, the higher degree of socio-relational information in complex social laughter types was linked to increases of connectivity between auditory association cortices, the right dorsolateral prefrontal cortex and brain areas associated with mentalizing as well as areas in the visual associative cortex. These modulations might reflect automatic analysis of acoustic features, attention direction to informative aspects of the laughter signal and the retention of those in working memory during evaluation processes. These processes may be associated with visual imagery supporting the formation of inferences on the intentions of our social counterparts. Here, the right dorsolateral precentral cortex appears as a network node potentially linking the functions of auditory and visual associative sensory cortices with those of the mentalizing-associated anterior mediofrontal cortex during the decoding of social information in laughter.
Highlights
Laughter is an evolutionary old communication signal with high relevance for social interactions [1]
As previous functional brain imaging studies on task-related effects during laughter perception were restricted to the perisylvian cortex, insula and amygdala [11,12] and did not report task-related activation changes in these brain regions, the results of our previous study were discussed in relation to task-induced effects in studies on the perception of other signals of nonverbal vocal communication of emotional information: Activations in the olIFG seem to reflect explicit evaluation of social information in the nonverbal vocal signal parallel to neuroimaging studies on perception of emotional speech melody [16,17,18,19,20,21,22], attention direction to emotional prosody [23], working memory for prosodic cues [24,25] and retrieval of memories associated with informative acoustic cues [26,27]
In contrast to the somewhat generic increase in connectivity between regions sensitive to complex social laughter types and the auditory cortex, a small number of connectivity increases outside the auditory cortex stand out distinctly. We propose that these increases in connectivity between anterior mediofrontal cortex, left occipito-temporal junction (L MOG) and right posterior superior temporal sulcus (R pSTS), on the one hand, and right dorsolateral prefrontal cortex (R pdIFG), on the other, may offer a perspective on the neurofunctional processes linking mentalizing (arMFC; [8,57,58,59,60], visual imagery (L MOG), explicit evaluation of social information in laughter (R pSTS) and auditory attention [23,61] and working memory processes [24,25,62,63] of auditory information, all linked to the dorsolateral prefrontal cortex
Summary
Laughter is an evolutionary old communication signal with high relevance for social interactions [1]. As previous functional brain imaging studies on task-related effects during laughter perception were restricted to the perisylvian cortex, insula and amygdala [11,12] and did not report task-related activation changes in these brain regions, the results of our previous study were discussed in relation to task-induced effects in studies on the perception of other signals of nonverbal vocal communication of emotional information: Activations in the olIFG seem to reflect explicit evaluation of social information in the nonverbal vocal signal parallel to neuroimaging studies on perception of emotional speech melody [16,17,18,19,20,21,22], attention direction to emotional prosody [23], working memory for prosodic cues [24,25] and retrieval of memories associated with informative acoustic cues [26,27]. PrMFC activation, on the other hand, appears consistent with the association of this region with focusing of attention and action monitoring [8,28,29,30,31]
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