ARTICLE

Laughter misunderstood: the consequences of integrating a many million years old reflex response into the cultural narrative.

Abstract

Wyndham Lewis described laughter as "the mind sneezing, and John Ray, "the hiccup of a fool". They were both correct in that laughing, sneezing and hiccuping are all reflexive behaviours. Laughter, whether reflexive or forced, is such a common phenomenon in human life that we have not been able to fully view it outside the cultural milieu. Even under the microscope of scientific scrutiny we have allowed the vernacular to intrude, leading to mistaken concepts and misdirect research. In the first part of this article I outline the probable origins of human laughter and highlight the mistakes to which humour researchers are prone. These include the use of the vernacular, top-down approaches that do not allow mapping from the neurophysiological aspects of laughter to the verbal structure of jokes, a misunderstanding of the relationship between empathy and sympathy and a  lack of a coherent explanation concerning the nature of pleasure and its manifestation during a laughter eliciting event. In the second part of the article the conclusions arrived at through a bottom-up approach are applied to the idea of intent. I challenge the common assumptions concerning intent in joking situations and question whether we really “get” jokes, laugh “at” jokes and people, and laugh “with” people.

Introduction

In this article I hypothesize that the laughter elicited by the processing of what we characterize as humorous events is an exapted vocal fight-or-flight displacement response. Exaptation is the process by which features acquire functions for which they were not originally adapted or selected. A displacement activity is a reaction to change (or anticipation of change) in activity, internal conflict, or motivational ambivalence (Schniter, 2001).    

The use of the term "displacement activity" in this article is in line with a slightly modified definition taken from A dictionary of Psychology (Oxford Uni Press): In ethology, the substitution of a [different] pattern of behaviour for behaviour that is appropriate to a particular situation, especially as a reaction to a conflict of motives. Male stickleback fish stand on their heads and dig into the sand as if building a nest when the impulses of attack and retreat are evenly balanced; fighting roosters often peck at the ground between bouts as though feeding; and humans often scratch their heads or perform self-grooming gestures when in a state of conflict, embarrassment, or stress. Also called displacement behaviour.      

The idea that a displacement behaviour is at the heart of laughter eliciting events is a bottom-up hypothesis that avoids the bogging down effect of competing humour theories and the contextual complexities of adult human laughter. It is the only hypothesis that I view as being able to give a meaningful explanation of the relationship that exists between laughter and the processing of events that cause its elicitation. It  allows the mapping of laughter eliciting events from laughter's neurological substrates, through physiological and behavioural effects,to the verbal constructs we have termed “jokes”.                                                                                                               As human laughter has its counterparts in the laughter-like behaviour in extant apes (Davila-Ross and Owren, 2009)  (Provine 1996), it is likely that the evolutionary forerunner of human laughter was of value in intraspecific interactions in great ape groups including our hominin ancestors. The circumstances in which chimpanzees "laugh" are limited to play-fighting, tickling and chasing, and although the "This is an attack /This is not really an attack" conflict may have laid the foundation for the joke format, it is obvious that the variety of circumstances in which humans laugh requires further explanation.                                                                                         The whole question appears to centre around the brain's processing of conflicting cognitions and emotions, and I propose that play-fight vocalization was exapted in the hominin line to include the disinhibition of the basic laughter response during decision making, particularly in fight or flight situations. As laughter predated language in our evolution, it is obvious that the laughter response was further exapted to deal with the conflicting cognitive and emotive responses to verbal constructs.                                                                                               When considering the nature of jokes, the space/time frame that should be applied extends further than the functioning of the individual’s brain that is processing them.The individual might comment that a joke made him laugh - the joke was the cause of the laughter, the joke preceded the laughter - but when we enlarge the space/time frame and consider the evolution of the systems in his brain that process the jokes, then the picture changes. We would not tell jokes if they did not give rise to laughter and a feeling we describe as pleasurable, which has been shown to accompany a decrease in stress levels and muscle tension. In fact, the word "joke" would not exist, as we distinguish the joke from a statement, story, puzzle or piece of nonsense, not only by the context in which it is delivered, but by its bodily effects. The laughter process preceded language in our evolution and so we can say it is the laughter process that is the "cause" of the joke in so far as the existence of the joke is dependent on the existence of the laughter process and its general form predetermined by the laughter process.

The origins of laughter

The psychologist, Davila-Ross and neuroscientist, Jaak Panksepp have both studied laughter in animals and associate the phenomenon with positive valence. The neural substrates of laughter elicitation, and physiological changes that occur during a joke telling event, contradict this assumption and suggest that basic laughter response should be viewed as being indicative of, and instrumental in, the modulation of a state of fear. Therefore, I define the basic neurological aspect of human laughter as the disinhibition of a stereotyped behaviour in response to the opposition or redundancy of the neural processes responsible for the expression of negative (fear based) behaviours. (A stereotypic behaviour is defined as a repetitive, invariant behaviour pattern with no obvious goal or function.)                                                                                                                                                       On an animal level, being chased and grasped is interpreted as an attack. In human play it is the awareness that the pursuer means no harm (This is an attack/This is not really attack) that gives rise to laughter. Our natural reaction to falling is fear, and yet young children often laugh heartily when they are tossed in the air and then caught by a trusted adult. In this case the children's laughter is an indication that the fear response is being opposed by their tacit knowledge that they are in no danger.                                                                                                         Laughter, or the neural processes that give rise to laughter-like vocalizations, appears to have been in the behavioural repertoire of apes for millions of years. New behaviours come about due to both physical and biological changes in an environment, and we must ask the question: What evolutionary pressures could have warranted the development of the phenomenon we have termed "laughter"?                                                                           There is a theory, one to which I subscribe, that the extant great apes began their evolution in Europe. There are very few fossil remains of great apes in Africa - only a few teeth which are thought to represent a species of gorilla and a species chimpanzee - but during the Miocene epoch (23.3-5.2 Ma) there were a large number of apes in Eurasia. A cooling climate may have caused the early European members of the great ape family (Hominidae) to migrate South into the warmer climes of Africa. Humans differ from other apes in having a fat layer just below the skin and can conserve heat through a countercurrent blood flow system in their extremities. Other than the aquatic ape theory, there is no explanation why such adaptations should have evolved in Africa. This leads to the possibility that the ape that gave rise to Homo was the last to enter Africa after exiting alone for some time in temperate conditions. Further pieces of evidence that point to an "into Africa" scenario is the fact that a fossil ape from Hungary, Rudapithecus, has large frontal sinuses (absent in Asian orangutans), brow ridges and a downwardly bent face, typical of extant African apes.                                                                                                                       The idea that laughter is an expression of positive valence ignores the fact that the most primitive form of laughter is exhibited during tickling. It is primitive in the facts that it is found in our ape relatives and is also a reflexive response. Reflex responses are not under conscious control and are usually associated with survival behaviours. This means that the response of our ape ancestors to being touched in a certain manner (similar to tickling) was extremely rapid and independent of the other senses and cognitive inputs that might have slowed down escape strategies. Such split second, reflex responses would have been of great survival value during ambush attacks and night time attacks by tree climbing predators.                                                                                            The laughter patterns of humans and chimpanzees are the most rhythmic and have the shortest intercall intervals of all the great ape species. However, whereas human laughter is voiced, chimpanzee laughter takes on the form of rapid panting. Why was the rapid panting of chimpanzees, and presumably the common ancestor of chimpanzees and humans, so important that it had to be encoded in their DNA?                                                Primates have a very long history of snake predation. This is inferred from the facts that monkeys have a specific alarm call for snakes and experiments have demonstrated a genetically based fear of snakes in monkey species. In 2011, German and Czechoslovakian researchers, working in Southern Germany, found 15 million year old fossilized vertebrae, which they calculated to be from a three and a half metre python, in. It is hardly likely they chanced upon the largest specimen of the largest constrictor species that existed in Europe at that time,and this find indicates the possibility of the existence of constrictor snakes capable of swallowing a medium sized primate. Constrictor snakes tighten their coils every time the prey breathes in, and it is possible that rapid panting disrupted this constriction process enough to allow the prey animal to wriggle free.                                           During the late Miocene cooling of Europe, large constrictor snakes either died out or migrated to warmer climates, and in some areas savannah-like grassland developed. This left our hominin ancestor with a stereotypic behaviour which I believe was vocalized and exapted to become a signal during play behaviour and also took on a mediating function in fight or flight situations.                                                                                                     Each habitat demands specific survival strategies from the animals that occupy it, and once our hominin ancestors began to spend time on the open grasslands emphasis would have been placed on certain behaviors. The strategies for food gathering and defense in the forest differ greatly from those on the grassland, where a change to a more omnivorous diet and a lack of immediately accessible escape routes would have meant the need for greater cooperation and a unifying system of control within the hominin bands. It is significant that the forest dwelling Bonobo chimpanzees live in loosely organized, female dominated groups (Stanford, C. 1998) but in line with most ground living primates, the hominins were probably led by a single experienced alpha male. In open country, it would have been essential for the alpha male to rapidly assess the severity of threats so as to deter any premature action on the part of individuals that might precipitate an aggressive response from potential predators. A novel event, or one perceived as potentially dangerous, would have induced a fear response in all the apes, including the alpha male, but in situations where no immediate fight or flight response was perceived by him as appropriate, an audible and contagious displacement activity would have been particularly effective in calming the members of the band and preventing panic scattering. Ramachandran (1998) characterizes this behaviour as communicating a "false alarm".   

The shortcomings of the three main humour theories  

The three main humour theories (the relief, incongruity resolved and aggression/superiority theories) cannot stand on their own as they only focus on particular stages and aspects of the sequence of events that take place during a laughter eliciting episode. Although aggressiveness and a feeling of superiority may be the motivations for telling a joke, and be woven into the jokes' content, this theory lacks any mechanism that would explain the elicitation of laughter. The relief theory is a "why?" theory, which merely highlights one function of laughter eliciting events - the lowering of stress- but offers no explanation of how this might occur. The incongruity theory is definitely a "how?" theory but it stops short of any real explanation when it is designated  the "incongruity resolved" theory. The explanation that the incongruity (conflict) is resolved, inducing a feeling of pleasure in the listener at being able to find a resolution, takes no cognizance of the fact that laughter is reflexive , nor the possibility that the feeling of pleasure could be a consequential rather than a subsequential  response to a joke. As the philosopher, William James expressed the idea - using the word "happy" instead of "feel pleasure" - "We don't laugh because we're happy – we're happy because we laugh."                                                                                                                                                                                                                                                                

The physiological effects of laughter eliciting events and the fight or flight response

I have little doubt that the basic form of laughter elicitation relies on the fear response being opposed in some manner.Even laughter that results from a joke telling event leaves physiological markers that link laughter to its ancient origins.Both a laughter inducing event and a "fight or flight" situation result in bodily arousal and a stimulation of the immune system, which is a normal response to both physical and psychological stress. During an episode of acute stress our bodies are readied to deal with any insult ensuing from the difficult circumstances in which we find ourselves - this includes the activation and release of large numbers of immune cells into the blood. Laughter has been reported to increase the numbers of natural killer and activated T cells, along with an increase in concentrations of immunoglobulins and gama interferon which help to fight infection and activate immune cells.(Berk and Tan 1996) In an earlier paper Berk reports a decrease in the blood levels of epinephrine (often called the fight or flight hormone) as a result of mirthful laughter, although in the majority of experiments dealing with the neurophysiological effects of laughter an increase in stress hormones has been detected. The reported levels of cytotoxic cells, neuroimmunologically active molecules and stress hormones in the blood vary so much from experiment to experiment that no specific conclusions can be made. Although we will have to wait until the inherent flaws in the various approaches are addressed, we can come to a general conclusion: the processing of a laughter eliciting event produces a muted physiological response typical of stress .Why should the telling of a joke, often in a relaxed atmosphere, lead to an immune response typical of a stress situation? The answer is that the processing conflict imposed by the joke mechanism mimics the motivational conflict typical of a "fight or flight" situation and leads to a similar, but muted, response. 

Fight or flight, laughter and displacement behaviours: the neurological connection

The number of brain areas that have been associated with mirthful laughter evoking events is large. They include the anterior cingulate cortex, the dorsolateral and medial ventral prefrontal cortex and orbitofrontal cortex, insular cortex, amygdala, basal ganglia, nucleus accumbens of the ventral striatopallidium, as well as the hypothalamus, the hippocampus, thalamus, the periaqueductal gray matter, the cerebellum, medulla and pons. (Biraben et al, 1999) (Heyd and Dolan, 2001) (Parvizi et al, 2001) (Wild et al, 2003).                                       Although many  of the brain areas above are concerned with language and the content of jokes, I am limiting my analysis to the systems that are most directly responsible for the disinhibition of laughter. First of all, I must make the distinction between Duchenne and non-Duchenne laughter. Duchenne laughter/smile, named after the French neurologist  Guillaume Duchenne, is seen as being involuntary (reflexive) whereas non-Duchenne laughter is a more controlled form of laughter which lacks an emotional basis. The diagram below (Fig 1) represents a rough representation of the difference between the two types of laughter.

Some writers (Decety and Moriguchi 2007) believe that the spindle neurons in the cingulate region of the cerebrum are involved in "judging the emotion in another person's gaze, to detection of intention in simple dynamic animations, attribution of intention to cartoons characters, story comprehension, detection of social transgression, and appreciation of humor."

Power and standing can be maintained by approval and respect, and only the fearful maintain power through aggression. Laughing at the less fortunate is not an act of the superior but of the frightened. We cannot inhibit the mental process we term empathy - it is an indispensable facet of comprehension - and because those people who laugh at the unfortunate cannot help putting themselves in the situation of those they belittle, the emotion behind their laughter is fear. These individuals have consciously distanced themselves from those they see as their inferiors; they do not sympathize with the less fortunate, but cannot escape the innate process of empathy, which places them in the very state they find repulsive.

The serotonergic system has strong anatomical and functional interactions with the dopaminergic system (Kapur & Remington, 1996). More specifically, a reciprocal interaction between these two systems has been proposed (Daw et al., 2002; Wong et al, 1995). Approach and withdrawal related behaviors are thought to be determined by the balance between dopamine and serotonin activity (Deakin & Graeff, 1991), with dopamine thought to encourage appetitive behaviors (Ikemoto & Panksepp, 1999) and serotonin thought to discourage appetitive behaviors and provoke withdrawal behaviors triggered by aversive stimuli (Daw et al, 2002).

In 2012 another group of European scientists found a hominid molar in  Bulgaria. Other fossils found with the molar ( those of giraffes, gazelles and antelopes) meant that great apes survived in Europe in savannah-like landscapes until seven million years ago.

Dopaminergic receptors may be involved in yawning as they are in Parkinson's disease and schizophrenia (Corio, 1990; Armbruster, 2009). It has been suggested that elevated levels of cortisol may decrease serotonin levels leading to depressive states (Dinan, 1994); and treatment of selective serotonin reuptake inhibitors (SSRI) have been well documented in conjunction with the side-effects of excessive yawning (Gutierrez-Alvarez, 2007). The effects of acute SSRI administration has been seen in healthy subjects through resulting HPA axis stimulation and increases in salivary cortisol levels (1-larmer, et al., 2003). Additional links have been made between cortisol secretion and SSRIs (Tucker, et al., 2004); and between serotonin and excessive yawning (Sommet, et al., 2007). Holmgren and colleagues (1992) considered serotonin as a positive modulator that possibly triggers the yawning response. Serotonin has been reported in diminished states in MS patients (Davidson, et al., 1977), and in stroke patients (Gao, et al., 2008).

It can be seen from the four quadrant model of mood, below, that pleasure is associated with the lowering of stress, and mental pain with the increasing of stress.

High arousal and high stress (anxiety),

High arousal and low stress (pleasant excitement),

Low arousal and high stress (boredom),

Low arousal and low stress .(relaxed drowsiness).

(After Cox and Griffiths 1995)

We report the most pleasure when arousal is increasing and stress is decreasing. Children will exhibit the exhilaration we have called "unbridled joy" when indulging in activities that cause a fear response which is quickly opposed by the knowledge/faith that they are in no danger; as when they are being chased or tossed about.

I view neither laughter (which is sometimes cited as an emotion in popular writing) nor exhilaration as emotive states. Laughter could in fact be viewed as anti-emotive as its evocation is instrumental in nullifying emotive activity, and exhilaration as a conscious appreciation of the effects of the hormones and neural transmitters that sustain arousal, again, when stress is decreasing. The same arousal state can be deemed to be pleasant or unpleasant depending on whether stress is decreasing or increasing. A first skydive only becomes exhilaratingly pleasant when you realize you are not going to die, and the mountaineer is only truly exhilarated when his goal is reached, and the arousal necessary for the attainment of his goal is separated from the stress engendered by the fear of failing or falling.

Although stress is sometimes, and erroneously, viewed in terms of arousal, the aspect of stress most pertinent to the study of laughing, crying and humor is stress in relation to action. Although the lay person may immediately associate emotions with feelings, feelings merely signal that neurohormonal changes are taking place. A distinction must be made between the motivation to action (emotive brain activity) and the appropriate bodily responses (arousal) to effectively carry it out. We enter a state of high stress when this neurohormonal readiness is maintained for long periods of time, or is continually being induced, but denied expression in action. We are in a continuous state of stress as the brain's cognitive mapping of the environment is matched by an emotive mapping, which interprets cognitions in terms of potential action. Emotive activity is taking place all the time as it is necessary for appropriate decision making in response to cognitions, but the brain works on a "need to know" basis, and because we associate emotion with specific feelings, for most of the time we do not appreciate that emotive processing is taking place.

Displacement activities and laughter   

In the introduction to this essay, displacement activities were associated with the following:

a) Motivational ambivalence

b) Anticipation of change in activity

c) Actual change in activity

d) Internal conflict

The effects of displacement activities have already been described in the introduction of this essay as: lowering stress during motivational conflict and nullifying persistent emotive brain states when rapidly changing stimuli have rendered them redundant. Laughter not only parallels displacement activities in being an effective alleviator of stress but occurs in all the circumstances described above.

a) Motivational ambivalence                     Example: The laughter of a young child being tossed in the air.

b) Anticipation of change in activity.    Example: The immediate laughter when a well known comedian                                                                                                      appears on a stage.

c) Actual change in activity.                      Example: Laughter of schoolchildren let out of class for playtime.

d) Internal conflict.                                       Example: Laughing at jokes.

It should also be noted here that there are parallels between laughter and a phenomenon already accepted as a displacement activity, yawning. (Schniter 2001) The contagious aspect of laughter and yawning suggests that earlier in our evolutionary development both acted to coordinate and modulate group behavior.

 laughter as a displacement activity

If laughter can be shown to be a displacement activity then I believe that the main conclusions arrived at in this article logically follow.                                                                                                                                                                         There are parallels between yawning - which is accepted to be a displacement activity - and laughter. In humans, laughing and yawning are contagious, stereotyped behaviours, and on a neurological level, both phenomena have been associated with the neurotransmitters serotonin and dopamine.                                                                                       Approach and withdrawal behaviours are considered  to be determined by the balance between dopamine and serotonin activity. Dopamine encouraging appetitive behaviours and serotonin discourages them and provokes withdrawal behaviours triggered by aversive stimuli. Although many neurotransmitters and areas of the brain contribute to the disinhibition of laughter a certain balance of dopamine and serotonin is required for laughter to take place. Displacement activities appear to be of two types those arising from conflicting motivational states and those arising from the physical or circumstantial blocking of positive actions. Laughter is of the first type, serotonin which is thought to inhibit escape acting in the area of the brain called the periaqueductal gray matter

Glial cell-derived neurotrophic factor, also known as GDNF GDNF has regenerative properties for brain cells and showed potential as treatment for Parkinson's disease when given the drug p patients were able to laugh again p shortage of dopamine

Drug Saf. 2007;30(4):327-31.

Drug-induced yawning: a review of the French pharmacovigilance database.

 Our work also indicates that stimulation of central dopamine or serotonin receptors elicits yawning in humans.

                                                                                          

Original Article

Citation: Translational Psychiatry (2013) 3, e298; doi:10.1038/tp.2013.66
Published online 3 September 2013

Depletion of serotonin in the basolateral amygdala elevates glutamate receptors and facilitates fear-potentiated startle
Open

L Tran1, B K Lasher2, K A Young3,4 and N B Keele1,2

Decrease sero produces fear. increase in sero blocks fear

Increase in dopa increases aggression   decrease in dopa lowers aggression. 

A Journal of Neurology

Neural correlates of laughter and humour



Best med 3

 Research examining how laughter influences stress hormones is somewhat conflicting. One early study looked at the results of viewing four different films on urinary excretion of epinephrine and norepinephrine in 20 female subjects.[11] The four films were chosen to elicit different emotions. The first was a natural-scenery film, which was expected to be very bland and not to elicit any strong emotions. A second film was funny, and elicited mirth and laughter. A third film was a war movie and was used to elicit feelings of tragedy and sadness. The fourth film was a horror story chosen to elicit anxiety. All of the subjects viewed each film and served as their own control mechanism in a pre-post-test design. Urinary hormone levels were measured during a 90 min control period before each film, during each film, and finally during a 90 min post-film session. Urinary epinephrine levels decreased significantly during the natural-scenery film (P < 0.01). Urinary epinephrine levels increased significantly during the war film (P < 0.05). Urinary epinephrine and norepinephrine both increased significantly during the humorous film (P < 0.05). Urinary epinephrine increased the most dramatically during the anxiety provoking film (P < 0.05), and norepinephrine levels also increased significantly during this film (P<0.001) see Figure 1.[11]

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