Laughter is in the air: involvement of key nodes of the emotional motor system in the anticipation of tickling

Abstract

In analogy to the appreciation of humor, that of tickling is based upon the re-interpretation of an anticipated emotional situation. Hence, the anticipation of tickling contributes to the final outburst of ticklish laughter. To localize the neuronal substrates of this process, functional magnetic resonance imaging (fMRI) was conducted on 31 healthy volunteers. The state of anticipation was simulated by generating an uncertainty respecting the onset of manual foot tickling. Anticipation was characterized by an augmented fMRI signal in the anterior insula, the hypothalamus, the nucleus accumbens and the ventral tegmental area, as well as by an attenuated one in the internal globus pallidus. Furthermore, anticipatory activity in the anterior insula correlated positively with the degree of laughter that was produced during tickling. These findings are consistent with an encoding of the expected emotional consequences of tickling and suggest that early regulatory mechanisms influence, automatically, the laughter circuitry at the level of affective and sensory processing. Tickling activated not only those regions of the brain that were involved during anticipation, but also the posterior insula, the anterior cingulate cortex and the periaqueductal gray matter. Sequential or combined anticipatory and tickling-related neuronal activities may adjust emotional and sensorimotor pathways in preparation for the impending laughter response.

Laughter as a paradigm of socio-emotional signal processing in dementia

“…Anteromedial prefrontal and anterior cingulate cortices behave as an integrated functional 'hub' in appraising the social value of heard laughter and disambiguating its social intent (44,45,91) and programming adaptive output behaviours, including own laughter and the subjective experience of mirth (92)(93)(94)(95)(96). Further correlates of overall laugher identi cation accuracy were identi ed here in closely structurally and functionally interconnected regions that are likely to be obligatorily engaged in appraising and responding to laughter: posterior insula, essential for integrating interoceptive information (97) and key acoustic cues that convey emotional content (98-101) during behavioural preparation; and mediodorsal thalamus, implicated in cognitive set shifting to meet changing behavioural contingencies (102).…”

Functional Neuroimaging of Human Hypothalamus in Socioemotional Behavior: A Systematic Review

“…Tickling-induced laughter is a quite old and conserved form of social physicality and communication allowing preverbal interaction between mother and infant and nonverbal communication between family, peers, and sexual partners. Tickling has been shown to induce positive affective responses [ 95 ] and to be significantly mediated by hypothalamic activity [ 41 , 96 ]. In healthy individuals, ticklish laughter induced by skin stimulation executed by a partner or a friend was associated with bilateral activation of the lateral hypothalamus along with other limbic areas such as the substantia nigra, amygdala, hippocampus, anterior insula, anterior cingulate gyrus, periaqueductal gray, and ventral tegmental area [ 41 , 96 ].…”

“…Tickling has been shown to induce positive affective responses [ 95 ] and to be significantly mediated by hypothalamic activity [ 41 , 96 ]. In healthy individuals, ticklish laughter induced by skin stimulation executed by a partner or a friend was associated with bilateral activation of the lateral hypothalamus along with other limbic areas such as the substantia nigra, amygdala, hippocampus, anterior insula, anterior cingulate gyrus, periaqueductal gray, and ventral tegmental area [ 41 , 96 ]. Activity in the lateral hypothalamus, the nucleus accumbens, and the ventral tegmental area was also observed in relation to anticipation of tickling, suggesting that these regions might support anticipatory mechanisms promoting social physicality [ 41 ].…”

“…In particular, we examined the involvement of the hypothalamus during affiliative, cooperative, as well as aggressive and antisocial interactions. We also considered studies investigating neural correlates of laughter, in particular ticklish laughter and humor, two highly rewarding behaviors tightly linked to socioemotional interaction and communication [ 39 , 40 , 41 ]. A concise description and analysis of the selected studies is first provided.…”

Uncover the Offensive Side of Disparagement Humor: An fMRI Study

“…Relative to N stimuli, DJ activated the anterior insula, the putamen, and the entorhinal cortex. These regions have been previously found to be activated during humor appreciation (Goel and Dolan, 2007;Kohn et al, 2011;Shibata et al, 2014;Caruana et al, 2015Caruana et al, , 2016Liu et al, 2019;Wattendorf et al, 2019;Talami et al, 2020). Interestingly, some neuroimaging studies found activations in the ACC and the anterior insula during the threats to another person's physical and social integrity (Beeney et al, 2011;Krach et al, 2011;Müller-Pinzler et al, 2016) and the left insula was also found activated in hostile jokes (Chan et al, 2016), suggesting that in DJ a feeling of mirth (and/or a desire to laugh) derived from the joke (e.g., SMA and precuneus) and the perception of the jokes' social inappropriateness (e.g., ACC and insula) coexist.…”