Content uploaded by Carolyn Mcgettigan
Author content
All content in this area was uploaded by Carolyn Mcgettigan on May 22, 2018
Content may be subject to copyright.
The social life of laughter
Sophie Scott, Nadine Lavan, Sinead Chen, and Carolyn McGettigan
Abstract
Laughter is often considered to be the product of humour. However laughter is a social emotion,
occurring most often in interactions, where it is associated with bonding, agreement, affection and
emotional regulation. Laughter is underpinned by complex neural systems, allowing it to be used
flexibly: in humans and chimpanzees, social (voluntary) laughter is distinctly different from
evoked (involuntary) laughter, a distinction which is also seen in brain imaging studies of
laughter.
Keywords
Emotion; voice; conversation; laughter; motor control
When do we laugh, and why?
Human beings are immersed in laughter: it is a pervasive non-verbal expression of emotion
(1,2), which is universally recognised (3), and is more like a different way of breathing than
a way of speaking (4) (see Box One). Laughter is mediated strongly by social context: we
are 30 times more likely to laugh if we are with someone else than if we are on our own (1,
2), and we laugh most of we can see and hear someone (even if this is via a computer)
compared to voice or text interactions (5). Laughter is also highly behaviourally contagious,
and can occur when primed solely by another’s laughter (2). Observational studies have
shown that laughter is commonly found in conversations, where it occurs at the rate of
around 5 laughs per 10 minutes of conversation (6). Strikingly, this is a much higher rate
than the amount of laughter that people self-report (6). Furthermore, if we are asked about
when we laugh, we report that we laugh at jokes and humour (1, 2): however, observational
studies show that not only does most laughter occur in conversations, within those
conversations most laughter is associated with statements and comments, rather than jokes
(1, 2, 6). Furthermore, in conversation, the person who laughs most frequently is the person
who has just spoken, indicating that laughter is frequently not a reaction to someone else’s
utterance (6). Much conversational laughter, therefore, is an intentional, communicative act.
For example, conversational laughter in both spoken and signed conversations is often timed
to occur at the end of utterances (1): this commonality across modalities underlines the
voluntary aspect of much of laughter production, since (at least in theory) a person could
simultaneously sign and laugh if she wished to.
Consistent with this emphasis on the social roles of laughter, researchers have suggested that
there are two different kinds of laughter, and that these are differentiated by how they are
elicited: the laughter can be either driven by outside events (reactive, involuntary laughter)
or be associated with a more intentional communicative act - i.e. more controlled, deliberate
Europe PMC Funders Group
Author Manuscript
Trends Cogn Sci. Author manuscript; available in PMC 2015 June 01.
Published in final edited form as:
Trends Cogn Sci. 2014 December ; 18(12): 618–620. doi:10.1016/j.tics.2014.09.002.
Europe PMC Funders Author Manuscripts Europe PMC Funders Author Manuscripts
laughter (7). This has been overtly compared to a distinction between spontaneous and
controlled smiling (7). Work with chimpanzees has revealed a similar distinction between
laughter which is generated in reaction to being tickled, versus laughter which is produced
during play (with the aim of making play last longer (8)).
Neural systems involved in the perception and production of laughter
The neural control of vocalization in humans is considered to involve two cortical systems
acting on midbrain and brainstem motor structures, where lateral premotor and motor sites
control the production of learned vocalizations such as speech and song, and a midline
system involving the anterior cingulate and supplementary motor area is associated with the
production of involuntary vocalizations, such as expressions of emotion (Jurgens, 2002).
Within this framework of voluntary and involuntary vocalizations, Wild et al. (2003) (10)
propose a model of laughter production, largely based on studies of pathological laughter, in
which they identify a coordinating centre for laughter in the brainstem comprising the
periaqueductal grey (PAG) and the upper reticular formation in the control of changes in
facial expressions, respiration, and vocalization. These structures are proposed to receive
excitatory inputs from cortical sites in the basal temporal and frontal lobes, as well as from
structures in the limbic system including the hypothalamus and basal ganglia. Here, the
lateral premotor cortices are implicated not in the basic production of laughter, but rather in
the suppression and regulation of spontaneous laughter vocalizations. In line with this view,
a recent neuroimaging study (11) found that the voluntary suppression of laughter during
tickling involved greater BOLD responses in lateral sensorimotor cortex compared with
when the participants were free to laugh when tickled (and when they voluntarily produced
laughter without tactile stimulation). Another key difference between voluntary and
(relatively) involuntary laughter in this study was a greater engagement of the hypothalamus
during tickling laughter (compared with voluntary or suppressed laughter), and an additional
correlation between activation in the PAG with the frequency of laughter episodes during
tickling. Both of these findings suggest a central involvement of these structures in the
production of basic, more automatic, expressions of positive experience.
Studies of the neural correlates of laughter perception have identified sensitivity to the social
significance of laughter signals. In a study of passive listening to emotional vocalizations
(12), sites on the lateral premotor and primary motor cortices showed a correlation with
valence, being greater to positive sounds (laughter and cheers of triumph) and lower for
negative sounds (screams of fear and expressions of disgust). This could reflect the
contagiousness of laughter and the greater tendency for positive vocalizations and associated
facial movements to occur in the context of social groups. However, more recent work (13)
showed that direct comparisons of the neural responses to voluntary and involuntary
laughter recordings gave no difference in motor cortex activation. Rather, the degree of
engagement of sensorimotor cortices when listening to both types of laughter was related to
individual differences in participants’ accuracy at classifying voluntary and involuntary
laughs and “posed” and “real”, respectively. This could be evidence that the listener engages
in some level of sensorimotor simulation as a mechanism for evaluating the social meaning
of heard vocalizations, rather than exhibiting a basic sound-to-action response. In the same
study, we observed preferential responses to involuntary laughter in bilateral auditory
Scott et al. Page 2
Trends Cogn Sci. Author manuscript; available in PMC 2015 June 01.
Europe PMC Funders Author Manuscripts Europe PMC Funders Author Manuscripts
cortex, while responses to voluntary laughs were greater in ventromedial prefrontal cortex.
This profile of auditory cortex engagement suggests that, on the one hand, there are acoustic
hallmarks that automatically register the presence of intense, “real” laughter in the brain of
the listener. In contrast, the absence or reduced prominence of such cues in voluntary laughs
engages mentalizing strategies in medial prefrontal cortex, to support the interpretation of
why the laugh has been produced, and what it means. Figure 1 summarizes the key sites
identified in studies of the production and perception of laughter.
Taking laughter seriously
Laughter is more than a positive emotional expression: its social use may extend to the
management of affective states within interactions. Laughter is one of the positive emotional
expressions which is expressly linked to a physiological reduction in the stressful reactions
to negative emotions (e.g. fear, anger, disgust), in a way which may be more effective than
other ways of managing negative emotions (e.g. suppression) (14, 15). Positive emotional
expressions have been associated with the down-regulation of negative emotions in
conversations between couples (14, 15): couples who reported the highest levels of marital
satisfaction also showed the most ‘skillful’ use of positive affect (e.g. laughter) to regulate
negative emotions during a difficult conversation (15). Laughter is therefore not simply a
common emotional vocalization, which we use to establish and maintain social bonds (1,2):
laughter may also simultaneously function as an essential behaviour for helping to ‘de-
escalate’ negative emotional experience, with a positive role in both the short term affective
state of the interaction, and the longer term state of relationships. Understanding the
behavioural and neurobiological bases of laughter will mean more than thinking about jokes:
it could provide a vital link between human language, relationships and emotional states.
References
1. Provine RR, Emmorey K. Laughter among deaf signers. J Deaf Stud Deaf Educ. 2006 Fall;11(4):
403–9. [PubMed: 16891353]
2. Provine RR. Laughing, tickling, and the evolution of speech and self. Current Directions in
Psychological Science. 2004; 13:215–218.
3. Sauter DA, Eisner F, Ekman P, Scott SK. The universality of human emotional vocalisations.
PNAS. 2010; 107(6):2408–12. [PubMed: 20133790]
4. Kohler KJ. ‘Speech-smile’, ‘speech-laugh’, ‘laughter’ and their sequencing in dialogic interaction.
Phonetica. 2008; 65(1-2):1–18. doi: 10.1159/000130013. [PubMed: 18523364]
5. Vlahovic TA, Roberts S, Dunbar D. Effects of Duration and Laughter on Subjective Happiness
Within Different Modes of Communication. Journal of Computer-Mediated Communication. 2012;
17(4):436–450.
6. Vettin J, Todt D. Laughter in conversation: Features of occurrence and acoustic structure. Journal of
Nonverbal Behavior. 2004; 28(2):93–115.
7. Gervais M, Wilson DS. The evolution and functions of laughter and humor: A synthetic approach.
Quarterly Review of Biology. 2005; 80(4):395–430. [PubMed: 16519138]
8. Davila-Ross M, Allcock B, Thomas C, Bard KA. Aping Expressions? Chimpanzees Produce
Distinct Laugh Types When Responding to Laughter of Others. Emotion. 2011; 11(5):1013–1020.
[PubMed: 21355640]
9. Jurgens U. Neural pathways underlying vocal control. Neuroscience and Biobehavioral Reviews.
2002; 26:235–258. [PubMed: 11856561]
Scott et al. Page 3
Trends Cogn Sci. Author manuscript; available in PMC 2015 June 01.
Europe PMC Funders Author Manuscripts Europe PMC Funders Author Manuscripts
10. Wild B, Rodden FA, Grodd W, Ruch W. Neural correlates of laughter and humour. Brain. Oct;
2003 126(Pt 10):2121–38. [PubMed: 12902310]
11. Wattendorf E, Westermann B, Fiedler K, Kaza E, Lotze M, Celio MR. Exploration of the Neural
Correlates of Ticklish Laughter by Functional Magnetic Resonance Imaging. Cerebral Cortex. Jun;
2012 23(6):1280–9. [PubMed: 22508768]
12. Warren JE, Sauter DA, Eisner F, Wiland J, Dresner MA, Wise RJ, Rosen S, Scott SK. (2006)
Positive emotions preferentially engage an auditory-motor “mirror” system. J Neurosci. Dec 13;
2006 26(50):13067–75. [PubMed: 17167096]
13. McGettigan C, Walsh E, Jessop R, Agnew ZK, Sauter DA, Warren JE, Scott SK. Individual
Differences in Laughter Perception Reveal Roles for Mentalizing and Sensorimotor Systems in the
Evaluation of Emotional Authenticity. Cereb Cortex. Aug 22.2013
14. Bloch L, Haase CM, Levenson RW. Emotion regulation predicts marital satisfaction: more than a
wives’ tale. Emotion. Feb; 2014 14(1):130–44. doi: 10.1037/a0034272. [PubMed: 24188061]
15. Yuan JW, McCarthy M, Holley SR, Levenson RW. Physiological down-regulation and positive
emotion in marital interaction. Emotion. Aug; 2010 10(4):467–74. doi: 10.1037/a0018699.
[PubMed: 20677864]
Scott et al. Page 4
Trends Cogn Sci. Author manuscript; available in PMC 2015 June 01.
Europe PMC Funders Author Manuscripts Europe PMC Funders Author Manuscripts
Box One
Breathing, speaking and laughing
Upper panel shows oscillograms for speech and laughter, middle panel shows
spectrograms for laughter and speech, lower panel shows chest expansion dynamics for
metabolic breathing, laughing and speaking. The time scale on the x axis is the same for
each (breathing, laughing and speaking). Both speaking and laughing are distinctly
different from metabolic breathing, in terms of chest wall movements. Laughter is
characterized by very rapid contractions of the intercostal muscles, resulting in large
exhalations followed by individual bursts of laughter: the spectral modulation of laughter
by supra-larangeal structures is minimal. Speech shows a fine pattern of intercostal
muscle movements, which are used to maintain constant sub-glottal pressure at the larynx
and to provide pitch and rhythm to the speech. Unlike laughter, speech also shows
considerable spectral complexity reflecting movements of the supra-laryngeal
articulators.
Scott et al. Page 5
Trends Cogn Sci. Author manuscript; available in PMC 2015 June 01.
Europe PMC Funders Author Manuscripts Europe PMC Funders Author Manuscripts
Figure 1. Voluntary and involuntary laughter in the brain
The coordination of human laughter involves periaqueductal gray and the reticular formation
with inputs from cortex, the basal ganglia and the hypothalamus [10]. The hypothalamus is
more active during reactive laughter than voluntary laughter [11]. Motor and premotor
cortices are involved in the inhibition of the brainstem laughter centres, and are more active
when suppressing laughter than when producing it [11]. Laughter perception involves
premotor cortex and SMA [12], while auditory and mentalizing regions showed differential
engagement by involuntary and voluntary laughter [13].
Scott et al. Page 6
Trends Cogn Sci. Author manuscript; available in PMC 2015 June 01.
Europe PMC Funders Author Manuscripts Europe PMC Funders Author Manuscripts