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The Social Life of Laughter Forum Trends in Cognitive Sciences December 2014, Vol. 18, No. 12 The social life of laughter 1 2 1 2 Sophie K. Scott , Nadine Lavan , Sinead Chen , and Carolyn McGettigan 1 Institute of Cognitive Neuroscience, UCL London, UK 2 Department of Psychology, Royal Holloway University of London, UK Laughter is often considered to be the product of humour. by how they are elicited: the laughter can be either driven However, laughter is a social emotion, occurring most by outside events (reactive, involuntary laughter) or be often in interactions, where it is associated with bonding, associated with a more voluntary communicative act – in agreement, affection, and emotional regulation. Laughter other words, more controlled, deliberate laughter [7]. This is underpinned by complex neural systems, allowing it has been overtly compared to the distinction between spon- to be used flexibly. In humans and chimpanzees, social taneous and controlled smiling [7]. Work with chimpanzees (voluntary) laughter is distinctly different from evoked has revealed a similar distinction between laughter which (involuntary) laughter, a distinction which is also seen is generated in reaction to being tickled versus laughter in brain imaging studies of laughter. which is produced during play (with the aim of making play last longer [8]). When do we laugh, and why? Neural systems involved in the perception and Human beings are immersed in laughter: it is a pervasive production of laughter non-verbal expression of emotion [1,2], which is universally The neural control of vocalization in humans is considered recognised [3], and results from spasms of diaphragm and to involve two cortical systems acting on midbrain and the intercostal muscles in the chest walls [4] (Box 1). brainstem motor structures, where lateral premotor and Laughter is mediated strongly by social context: we are motor sites control the production of learned vocalizations 30-fold more likely to laugh if we are with someone else such as speech and song, and a midline system involving than if we are on our own [1,2], and we laugh most if we can the anterior cingulate and supplementary motor area that see and hear someone (even if this is via a computer) is associated with the production of involuntary vocaliza- compared to voice or text interactions [5]. Laughter is also tions, such as expressions of emotion [9]. Within this highly behaviourally contagious, and can occur when framework of voluntary and involuntary vocalizations, primed solely by another’s laughter [2]. Observational Wild et al. [10] propose a model of laughter production, studies have shown that laughter is commonly found in largely based on studies of pathological laughter, in which conversations, where it occurs at the rate of 5 laughs per they identify a coordinating centre for laughter in the 10 minutes of conversation [6]. Strikingly, this is a much brainstem comprising the periaqueductal grey (PAG) higher rate than the amount of laughter that people self- and the upper reticular formation in the control of changes report [6]. Furthermore, if we are asked about when we in facial expressions, respiration, and vocalization. These laugh, we report that we laugh at jokes and humour [1,2]; structures are proposed to receive excitatory inputs from however, observational studies show that not only does cortical sites in the basal temporal and frontal lobes, as most laughter occur in conversations, but within those well as from structures in the limbic system including the conversations most laughter is associated with statements hypothalamus and basal ganglia. In this case the lateral and comments rather than with jokes [1,2,6]. Furthermore, premotor cortices are implicated not in the basic produc- in conversation, the person who laughs most frequently is tion of laughter but rather in the suppression and regula- the person who has just spoken, indicating that laughter is tion of spontaneous laughter vocalizations. Further frequently not a reaction to someone else’s utterance studies will be able to determine the extent to which the [2,6]. Much conversational laughter, therefore, is a volun- PAG is involved in laughter because of its affective role, or tary, communicative act. For example, conversational because of the importance of the PAG in the production of laughter in both spoken and signed conversations is often vocal behaviour more widely. Furthermore, establishing timed to occur at the end of utterances [1]: this commonal- the role of the lateral speech motor areas in conversational ity across modalities underlines the voluntary aspect of laughter, in addition to the suppression of laughter, will some laughter because (at least in theory) a person could be important to determine the extent to which conversa- simultaneously sign and laugh if she wished to. tional laughter is part of a more voluntary vocalization Consistent with this emphasis on the social roles of system or whether laughter is always driven by midline laughter, researchers have suggested that there are two neural systems. For example, a recent neuroimaging study different kinds of laughter, and that these are differentiated [11] found that the voluntary suppression of laughter during tickling involved greater blood oxygen level-depen- dent (BOLD) responses in lateral sensorimotor cortex Corresponding author: Scott, S.K. ([email protected]) Keywords: emotion; voice; conversation; laughter; motor control. compared with when the participants were free to laugh 1364-6613/ when tickled (and when they voluntarily produced laugh- ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tics.2014.09.002 ter without tactile stimulation). This same study [11] found that a key difference between voluntary and (relatively) 618 Forum Trends in Cognitive Sciences December 2014, Vol. 18, No. 12 Box 1. Metabolic breathing, speaking, and laughing Both speaking and laughing require distinctly different control of the supra-laryngeal structures is minimal. Speech shows a fine pattern intercostal muscles, seen in the lower panel of Figure I as changes in of intercostal muscle movements, which are used to maintain chest wall movements, compared to the profile of metabolic constant sub-glottal pressure at the larynx and to provide pitch and breathing. Laughter is characterized by very rapid contractions of rhythm to the speech. Unlike laughter, speech also shows consider- the intercostal muscles, resulting in large exhalations followed by able spectral complexity, reflecting movements of the supra- individual bursts of laughter: the spectral modulation of laughter by laryngeal articulators. Laughter Speech 0.127 Amplitude (Pa) Frequency (Hz) Chest expansion (mV) –0.127 10000 Metabolic breathing 0 15 –15 0 Time (s) 12 0 Time (s) 12 0 Time (s) 12 TRENDS in Cognitive Sciences Figure I. Metabolic breathing, speaking, and laughing. The upper panel shows oscillograms for speech and laughter, the middle panel shows spectrograms for laughter and speech, and the lower panel shows chest expansion dynamics for metabolic breathing, laughing, and speaking. The timescale on the x axis is the same for each (breathing, laughing, and speaking). involuntary laughter was a greater engagement of the engages in some level of sensorimotor simulation as a hypothalamus during tickling laughter (compared with mechanism for evaluating the social meaning of heard voluntary or suppressed laughter). It also demonstrated vocalizations, rather than exhibiting a basic sound-to-action a correlation between activation in the PAG with the response. In the same study, we observed preferential frequency of laughter episodes during tickling. responses to involuntary laughter in bilateral auditory Studies of the neural correlates of laughter perception cortex, whereas responses to voluntary laughs were have identified sensitivities to the social significance of greater in ventromedial prefrontal cortex. This profile of laughter signals. In a study of passive listening to emo- auditory cortex engagement suggests that, on the one hand, tional vocalizations [12], sites on the lateral premotor and there are acoustic hallmarks that automatically register the primary motor cortices showed a correlation with valence, presence of intense, ‘real’ laughter in the brain of the listen- being greater to positive sounds (laughter and cheers of er. On the other hand, the absence or reduced prominence triumph) and lower for negative sounds (screams of fear of such cues in voluntary laughter engages mentalizing and expressions of disgust). This could reflect the con- strategies in medial prefrontal cortex to support the inter- tagiousness of laughter and the greater tendency for posi- pretation of why the laughter has been produced, and tive vocalizations and associated facial movements to occur what it means. Figure 1 summarizes the key sites identified in the context of social groups. However, more recent work in studies of the production and perception of laughter. [13] showed that direct comparisons of the neural responses to voluntary and involuntary laughter record- Taking laughter seriously ings gave no difference in motor cortex activation. Instead, Laughter is more than a positive emotional expression: its the degree of engagement of sensorimotor cortices when social use may extend to the management of affective listening to both types of laughter was related to individual states within interactions. Laughter is one of the positive differences in the accuracy of the participants in classifying emotional
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