The Neurology of Humour
Posted in Clinical Review Article on 4th Feb 2014
- Functional imaging in the normal brain has implicated distributed cortical and subcortical networks in processing different aspects of humour perception and comprehension with separable cognitive, affective and social dimensions
- Impaired appreciation of humour is a feature of diverse developmental and acquired brain disorders
- Humour may present a useful model for studying certain complex behavioural functions of high clinical relevance: these include the resolution of ambiguity and incongruity, mentalising and empathy
A neurologist, a neurosurgeon and a psychiatrist walk into a bar.
The barman says, ‘Is this some kind of joke?’
A sense of humour is among our most cherished attributes. It eases the daily grind, promotes amity with our fellows and may even salve our hurts1 or confer reproductive success.2 Laughter might be ‘the shortest distance between two people’, as averred by Victor Borge; avowedly humourless societies tend to disintegrate (think of Nazi Germany) and humour is feared by tyrants of all persuasions. In its more refined forms it is held up as a mark of discernment, but there can be very few of us who have not, from time to time, been reduced to fits of helpless mirth even in highly unsuitable situations. This underlines the extraordinary range and power of humour in its many genres. Despite its ubiquity as a phenomenon, the peculiarities of humour are often closely bound to time and place; the jokes of Euripides and Shakespeare have travelled less well than their tragedies and tastes in humour are heavily socially and culturally sanctioned.3 On the other hand, certain humour motifs may be truly universal: from an evolutionary perspective, laughter is probably older than language4 and the destabilising properties of fruit peel were probably already drawing uncharitable sniggers among our cave-dwelling forebears. Though it is not clear that other animals possess humour, it is perhaps relevant that analogues of laughter and smiling in our primate relatives signal aggression or threat.5
In addition to its social and existential virtues, humour is of considerable interest as a cognitive neuropsychological phenomenon. Jokes typically entail the opposition of apparently incongruous elements that must be resolved in a surprising way.6 These operations entail a number of cognitive processing stages and components. The process of resolution requiring the integration of conflicting alternatives is a model of frontal lobe function,7 while the emotional pay-off suggests an analogy with other phenomena (such as music) that link psychological expectancies with the brain mechanisms of reward.8 However, the neurobiological basis of humour remains largely obscure and the effects of brain disease on humour processing are poorly understood. Neurologists have taken an interest in the more extreme outward manifestations (like pathological affect and fou rire prodromique)9 while largely ignoring the cognitive machinery behind them. Here we argue that this is a wasted opportunity, using examples in which alterations of humour are integral to neurological disease. We do not, however, wish to minimise the challenges inherent in attempting to study the neurology of humour.10,11,12 There is presently no standard, widely accepted cognitive model of humour processing, nor indeed any agreed terminology of the processes involved.10 Caution is therefore required in interpreting the published literature and this is compounded by the diversity of stimuli and paradigms that have been used to assess humour processing in health and disease.11,12 Furthermore, as is the case for all complex, multi-component cognitive processes, functional neuroimaging studies of humour (which delineate all brain areas involved in the relevant process) must be reconciled with clinical lesion studies (which identify areas critical for the process). In functional imaging work it is not always clear which contrasts should be employed to isolate specific components of humour processing and most imaging modalities lack the temporal resolution to capture the temporal staging of these components (this typically requires electrophysiological techniques).
In this review we highlight the many gaps in our current understanding of the neurology of humour and propose a framework for the systematic clinical analysis of humour cognition. Our focus here is on the brain mechanisms that process humour and the disorders that affect humour processing, rather than pathological affect and abnormal laughter, which are already well reviewed.13
Humour and the healthy brain
What happens in the brain when we ‘get’ a joke? Functional imaging studies in the healthy brain using stimuli as diverse as one-liners, sight gags, captionless cartoons, comic strips, Seinfeld, The Simpsons and stand-up comedy videos have implicated distributed cortical and subcortical networks in processing different aspects of humour perception and comprehension with separable cognitive, affective and social dimensions of the brain’s response. The temporo-parietal junction is engaged in the cognitive analysis of potentially humorous stimuli:14 this is consistent with a proposed role for this region in bringing stored expectations online7 and for processing socially relevant information more generally.15 This may be particularly pertinent to the basic humour associated with physical comedy (slapstick), which relies on the violation of physical or social norms. More widespread brain regions including posterior inferior temporal, inferior frontal and premotor cortices, limbic structures such as the insula and amygdala and subcortical structures including nucleus accumbens, putamen, thalamus and cerebellum are more specifically involved in detecting and appreciating incongruity and accompanying emotions of surprise and delight.7,12,16,17 While these processes are generally intimately intertwined and difficult to separate using imaging paradigms,18 they are dissociable; humorous intent can be recognised even when it does not provoke amusement. The onset of laughter has been taken to signal the dawning of amusement, associated with insula and amygdala activation;7 while degree of amusement (funny contrasted with unfunny jokes) has been correlated with activation in ventral prefrontal, anterior cingulate, superior and mid temporal cortices and limbic and dopaminergic reward networks including ventral striatum and nucleus accumbens.12,16,19 Electrophysiological techniques may allow dissection of the temporal dynamics of joke comprehension.11
There is some evidence for separable neural correlates of different kinds of humour. Puns engage components of a phonological processing network including the left inferior frontal gyrus whereas semantic jokes engage regions including the posterior temporal lobe which are involved in semantic integration.12 Pictorial cartoons recruit areas mediating visual imagery19 whereas those requiring inference on mental states particularly engage brain regions concerned with mentalising or ‘theory of mind’.14 The process of incongruity resolution associated with sarcasm detection activates brain networks engaged in language processing and mentalising.20 While the brain basis for idiosyncratic tastes in humour is likely to remain obscure, responses may be modulated by gender21 and personality.22 Individual variation in sense of humour (ability to grasp one-liners) has been correlated with electrophysiological markers including lateralised frontal evoked potentials that may index frame-shifting and surprise.11
Brain disorders and humour
Various brain disorders have been linked to disturbed understanding or appreciation of humour. Aside from their clinical relevance, such disturbances can (as with other complex neuropsychological functions) potentially reveal underlying critical brain substrates and cognitive architecture. However, much early work on the neurology of humour draws on a very broad anatomical distinction between the right and left cerebral hemispheres.23,24 Damage involving the non-dominant hemisphere (particularly the frontal cortex and anterior temporal lobe) often degrades the appreciation of humour;10,23 in these patients, amusement dissociates from comprehension of jokes, perhaps reflecting a more general deficit in linking cognitive with appropriate emotional responses. Some patients with right hemisphere damage find humour in intrinsically humourless situations.23 Damage involving right frontal polar cortex impairs appreciation of more sophisticated jokes while leaving responses to slapstick scenarios largely unscathed,10 perhaps reflecting an inability to resolve incongruity in novel contexts. It is our clinical impression that patients with frontotemporal dementia chiefly involving the right hemisphere have somewhat similar difficulties; particularly in the context of mesio-orbital frontal involvement, such patients may exhibit reduced comprehension of sarcasm25 and frequent prankish joking and punning (Witzelsucht)26 though the onset of the disorder may be signalled by a more subtle predilection for comic strips, slapstick or scatological jokes (a coarsening of comedic tastes that may have parallels in the culinary or musical realms). More specifically verbal jokes appeared to rely on the ability to set shift and verbal abstraction whereas the performance in cartoons was more reliant on attention to details and the ability to visually search the scene.10
Patients with focal damage restricted to a particular cerebral hemisphere show characteristic profiles of deficits for particular components of humour processing.24 Whereas patients with right hemisphere damage may be unable to discriminate between punchlines and non sequitur endings to jokes, those with left hemisphere damage tend to prefer coherent but unsurprising (and unfunny) endings. Individuals with agenesis of the corpus callosum may also have particular difficulty with narrative jokes, perhaps because these depend on inter-hemispheric integration of linguistic and non-literal metaphorical dimensions.27 Right hemisphere damage seems more likely to be associated with impaired ability to mentalise (theory of mind), while left hemisphere damage is more likely to affect the comprehension of humour that does not rely on mental inferences.28 A mentalising defect is also likely to contribute to degraded humour processing in frontotemporal dementia.25
Impaired appreciation of humour is a feature of diverse developmental and acquired disorders with more diffuse brain dysfunction, including autism spectrum disorders,29 schizophrenia,30 amyotrophic lateral sclerosis,31,32 traumatic brain injury,33 and Tourette’s syndrome.34 Orbitofrontal cortex dysfunction may be a common theme linking these disorders with cases of focal brain damage and network disintegration in frontotemporal dementia. Certain disorders may produce specific cognitive deficits that impact on humour processing. The difficulty shown by patients with schizophrenia in interpreting sarcasm may at least partly reflect pitch processing difficulties35 while impaired mentalising in social phobia or Asperger’s syndrome impairs understanding of humour that depends on theory of mind, but not visual jokes or puns.29 There have been few functional neuroimaging studies of humour processing in brain disease; in one fMRI study with cartoon stimuli, individuals with cataplexy compared with healthy controls had heightened activation of subcortical reward circuitry, but in addition, increased engagement of ‘inhibitory’ circuitry in right inferior frontal gyrus, suggesting an intriguing disease model for the common experience of struggling to regain composure when we are ‘weak’ with laughter.36
In Table 1, we present a simplified framework for assessing humour cognition that summarises functional neuroimaging evidence concerning the brain basis of humour with proposed clinical associations requiring substantiation in further work.
Observations such as these in the healthy and damaged brain should encourage neurologists to enquire more systematically about their patients’ humour sensibilities and for cognitive scientists to develop frameworks that can reconcile lesion and functional neuroimaging work. It is clear that humour, as an aspect of brain function, is multi-dimensional and highly distributed. Admittedly no single cognitive model is ever likely to subsume the double entendres of Benny Hill, the acerbic social commentary of Peter Cook or Woody Allen, the sparkling wordplay of Wilde and Moliere, the whimsical meanderings of Peanuts. Nevertheless, humour may present a useful model for studying certain complex behavioural functions of high clinical relevance: these include the resolution of ambiguity and incongruity, mentalising and the exercise of empathy;18 and the putative ‘lexicon’ of jokes (particularly slapstick scenarios) that may be laid down in early childhood.37 These different dimensions of humour processing might be probed by customised stimuli that control for potentially confounding surface characteristics (for example, Figure 1). More broadly, if humour serves to debug inferential errors in our comprehension of the world,1 it might turn out to have a key role in the maintenance of cognitive well-being: perhaps the enduring appeal of Rabelais, the Pythons and Dali’s Aphrodisiac Telephone reflect such neural housekeeping by the absurd and the surreal.
If it seems ironic to have two neurologists write on humour, perhaps a more compelling lead lies with literature, which is replete with melancholy clowns and the wisdom of fools. We hope the neuroscientific study of humour will help us to a better understanding of our patients and the predicaments they face, which do, after all, encompass some of the more grim and bitter ironies of medical practice.
1. Hurley MM, Dennett DC, Reginald BA. Inside Jokes: using humor to reverse-engineer the mind. Cambridge, Massachusetts: MIT Press; 2011.
2. Bressler ER, Balshine S. The influence of humor on desirability. Evol Hum Behav 2005;27:29-39.
3. Holmes J, Marra M. Humour as a discursive boundary marker in social interaction. In: Duszak A, editor. Us and Others: Social Identities Across Languages, Discourses and Cultures. Amsterdam: John Benjamins Publishing Company; 2002.
4. Hayworth D. The social origins and functions of laughter. Psychological Review 1928;35:367-84.
5. De Waal FB. Darwin’s legacy and the study of primate visual communication. Ann N Y Acad Sci 2003;1000:7-31.
6. Suls J. A two-stage model for the appreciation of jokes and cartoons: an information-processing analysis. Goldstein PE, McGhee JH, editors. New York: Academic Press; 1972. 81–100 p.
7. Moran JM, Wig GS, Adams RB, Jr., Janata P, Kelley WM. Neural correlates of humor detection and appreciation. Neuroimage 2004;21:1055-60.
8. Lehne M, Rohrmeier M, Koelsch S. Functional neuroimaging of tension: A study with music. Soc Cogn Affect Neurosci 2013.
9. Fere MC. Le fou rire prodromique. Rev Neurol 1903;11:353-8.
10. Shammi P, Stuss DT. Humour appreciation: a role of the right frontal lobe. Brain 1999;122(Pt 4):657-66.
11. Coulson S, Kutas M. Getting it: human event-related brain response to jokes in good and poor comprehenders. Neurosci Lett 2001;316:71-4.
12. Goel V, Dolan RJ. The functional anatomy of humor: segregating cognitive and affective components. Nat Neurosci 2001;4:237-8.
13. Lauterbach EC, Cummings JL, Kuppuswamy PS. Toward a more precise, clinically-informed pathophysiology of pathological laughing and crying. Neurosci Biobehav Rev 2013;37:1893-916.
14. Samson AC, Zysset S, Huber O. Cognitive humor processing: different logical mechanisms in nonverbal cartoons–an fMRI study. Soc Neurosci 2008;3:125-40.
15. Schurz M, Aichhorn M, Martin A, Perner J. Common brain areas engaged in false belief reasoning and visual perspective taking: a meta-analysis of functional brain imaging studies. Front Hum Neurosci 2013;7:712.
16. Mobbs D, Greicius MD, Abdel-Azim E, Menon V, Reiss AL. Humor modulates the mesolimbic reward centers. Neuron 2003;40:1041-8.
17. Wild B, Rodden FA, Rapp A, Erb M, Grodd W, Ruch W. Humor and smiling: cortical regions selective for cognitive, affective, and volitional components. Neurology 2006;66:887-93.
18. Bartolo A, Benuzzi F, Nocetti L, Baraldi P, Nichelli P. Humor comprehension and appreciation: an FMRI study. J Cogn Neurosci 2006;18:1789-98.
19. Watson KK, Matthews BJ, Allman JM. Brain activation during sight gags and language-dependent humor. Cereb Cortex 2007;17:314-24.
20. Uchiyama H, Seki A, Kageyama H, Saito DN, Koeda T, Ohno K, Sadato N. Neural substrates of sarcasm: a functional magnetic-resonance imaging study. Brain Res 2006;1124:100-10.
21. Azim E, Mobbs D, Jo B, Menon V, Reiss AL. Sex differences in brain activation elicited by humor. Proc Natl Acad Sci U S A 2005;102:16496-501.
22. Mobbs D, Hagan CC, Azim E, Menon V, Reiss AL. Personality predicts activity in reward and emotional regions associated with humor. Proc Natl Acad Sci U S A 2005;102:16502-6.
23. Gardner H, Ling PK, Flamm L, Silverman J. Comprehension and appreciation of humorous material following brain damage. Brain 1975;98:399-412.
24. Bihrle AM, Brownell HH, Powelson JA, Gardner H. Comprehension of humorous and nonhumorous materials by left and right brain-damaged patients. Brain Cogn 1986;5:399-411.
25. Kipps CM, Nestor PJ, Acosta-Cabronero J, Arnold R, Hodges JR. Understanding social dysfunction in the behavioural variant of frontotemporal dementia: the role of emotion and sarcasm processing. Brain 2009;132:592-603.
26. Lishman WA. Organic Psychiatry: The Psychological Consequences of Cerebral Disorder. 3rd ed. United Kingdom: Blackwell Publishing; 2003.
27. Brown WS, Paul LK, Symington M, Dietrich R. Comprehension of humor in primary agenesis of the corpus callosum. Neuropsychologia 2005;43:906-16.
28. Gallagher HL, Happe F, Brunswick N, Fletcher PC, Frith U, Frith CD. Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks. Neuropsychologia 2000;38:11-21.
29. Samson AC, Hegenloh M. Stimulus characteristics affect humor processing in individuals with Asperger syndrome. J Autism Dev Disord 2010;40:438-47.
30. Corcoran R, Cahill C, Frith CD. The appreciation of visual jokes in people with schizophrenia: a study of ‘mentalizing’ ability. Schizophr Res 1997;24:319-27.
31. Girardi A, Macpherson SE, Abrahams S. Deficits in emotional and social cognition in amyotrophic lateral sclerosis. Neuropsychology 2011;25:53-65.
32. Staios M, Fisher F, Lindell AK, Ong B, Howe J, Reardon K. Exploring sarcasm detection in amyotrophic lateral sclerosis using ecologically valid measures. Front Hum Neurosci 2013;7:178.
33. Braun CM, Lussier F, Baribeau JM, Ethier M. Does severe traumatic closed head injury impair sense of humour? Brain Inj 1989;3:345-54.
34. Eddy CM, Mitchell IJ, Beck SR, Cavanna AE, Rickards H. Social reasoning in Tourette syndrome. Cogn Neuropsychiatry 2011:1-22.
35. Kantrowitz JT, Hoptman MJ, Leitman DI, Silipo G, Javitt DC. The 5% difference: early sensory processing predicts sarcasm perception in schizophrenia and schizo-affective disorder. Psychol Med 2013:1-12.
36. Reiss AL, Hoeft F, Tenforde AS, Chen W, Mobbs D, Mignot EJ. Anomalous hypothalamic responses to humor in cataplexy. PLoS One 2008;3:e2225.
37. Goel V, Dolan RJ. Social regulation of affective experience of humor. J Cogn Neurosci 2007;19:1574-80.
ACNR 2014;V13(7):9-11. Online 4/2/14Download this Article