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.

Introduction

Laughter is an evolutionary old communication signal with high relevance for social interactions [1]. Tickling laughter is thought to be a more reflex-like behavior confined to the context of tickling and play which enforces play behavior and social bonding [2]. This laughter type is already present in non-human primates [3]. In humans, laughter has diversified beyond the primordial reflex-like laughter which is induced by tickling or play and which is related to play maintenance [4] and encompasses laughter types with both more complex social functions and positive as well as negative connotations (e.g., joy or taunt). The term “complex social laughter” refers to the fact that, in contrast to tickling laughter, these laughter types are produced in a wide variety of social situations and can be used in a conscious and goal-directed manner to influence and modify the attitudes and behaviors of our social counterparts [5], [6].

In a previous report based on the same fMRI data set as the present study and focusing on temporal and frontal brain regions [7], we delineated brain areas associated with the perception of these presumably evolutionary different laughter types. Complex social laughter types (CSL, i.e., joyful and taunting laughter) which were termed “emotional” laughter types in our previous report [7] elicited stronger cerebral responses in the anterior rostral mediofrontal cortex (arMFC) known to be activated during mentalizing tasks (i.e., inferring states of minds or intentions, [8]). Tickling laughter, in contrast, led to a stronger activation of the auditory association cortex presumably reflecting the higher acoustic complexity of the rapid and high-pitched tickling laughter [9] (see also Table S1). Similar activations of the auditory cortex have been described in connection with the perception of affective vocalizations including laughter [5], [10]–[13] and were found to be stronger for laughter as compared to speech [14]. In the neighboring research area of emotional prosody perception, stronger activations for emotional as compared to neutral speech melody have been demonstrated to be significantly associated with acoustic complexity [15]. Additionally, task-related focusing on the social information in the laughter signal increased activation in the orbitolateral part of the inferior frontal gyrus (olIFG) as well as the posterior rostral mediofrontal cortex (prMFC). 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]–[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]–[31].

Recently, the notion that the neural substrates of cognitive functions in health and disease are also reflected in dynamic changes of connectivity between distinct and often distant brain regions has been supported by a fast growing amount of empirical evidence [32], [33]. In the area of speech comprehension and production, first attempts have been made to delineate patterns of brain connectivity underlying these cognitive functions [34]. With regard to non-verbal vocal cues (e.g., laughter or speech melody) available data is scarce: Ethofer and colleagues found evidence for a parallel flow of information within regions sensitive to explicit evaluation of emotional prosody from the right posterior temporal cortex to the bilateral olIFG using dynamic causal modeling [19]. In a recent study, Leitman and colleagues [35] described a frontotemporal network for processing of emotional prosody where cue saliency inversely modulated connectivity between the right IFG and the auditory processing regions in the right middle/posterior superior temporal cortex. With respect to the perception of laughter, to our knowledge only one study of brain connectivity [36] has been performed previously. Here, laughter and crying were used as nonverbal affective stimuli in contrast to control sounds. No previous study, however, addressed different types of laughter specifically.

Therefore, it was the aim of the present fMRI study to investigate modulations of neural connectivity between brain regions engaged in the perception of different types of laughter (i.e., joyful, taunting and tickling) to further elucidate the underpinnings of the neural processing of different aspects of the laughter signal (i.e., complexity of socio-relational content and acoustic complexity) and of different states of attention with regard to the social information carried in the laughter signal employing psycho-physiological interaction (PPI) analyses [37], [38]. Attention allocation towards or away from social information in laughter was modulated by two different tasks (i.e., laughter type categorization and laughter bout counting).

Based on the presently sole pertinent PPI analysis by Leitman and colleagues [35], we cautiously hypothesized that the lower degree of complex social information of tickling laughter, when interpreted as a lower degree of cue saliency when compared to CSL, would be associated with stronger connectivity between the right IFG and the right middle/posterior superior temporal gyrus (STG). A second tentative hypothesis was based on the study of Ethofer and colleagues [19] demonstrating flow of information among regions with stronger responses during explicit evaluation of emotional prosody. As the increased responses during laughter type categorization observed in the right pSTS and bilateral olIFG in our previous analysis [7] bear a striking resemblance to the activations observed by Ethofer and colleagues, we hypothesized that the explicit evaluation of social information in laughter would increase the connectivity between the right pSTS and bilateral olIFG. Finally, based on previous research indicating activation of the bilateral amygdalae through laughter [11]–[13], we defined this region as an additional region of interest for our analyses of hemodynamic activation and connectivity.