The Psychobiology of Humor and Laughter

ch006-P372564.qxd 15/8/06 10:02 AM Page 153 CHAPTER 6 The Psychobiology of Humor and Laughter Like all psychological phenomena, humor is based on a large number of complex biological processes taking place in the brain and nervous system. To experience humor, an individual must first perceive playful incongruity in a stimulus event. This perceptual process draws on systems located in many regions of the cerebral cortex involved in visual and auditory perception, lan- guage comprehension, social cognition, logical reasoning, and so forth. When humor is perceived, these cognitive processes stimulate emotional systems associated with positive feelings of mirth and amusement, involving areas in the prefrontal cortex and limbic system. These emotion systems also release a cocktail of biochemical mole- cules, producing further changes in the brain and throughout the body via the autonomic nervous system and endocrine system. In addition, the activation of mirthful emotion typically triggers the expressive responses of smiling and laughter, which involve the brainstem and its connections to the forebrain, as well as nerves leading to muscles in the face, larynx, and respiratory system. The investigation of these sorts of biological processes in humor lies within the domain of biological psychology (also known as psychobiology or physiological psychology), the branch of the discipline that studies the relation between behavior and the body, particularly the brain. Biological psychology is part of a broader field of study known as neuroscience, which also includes disciplines such as neurophysi- ology, neuroanatomy, and brain biochemistry. Although the study of humor and laughter has not been a major focus in biological psychology, there has been a small 153 ch006-P372564.qxd 15/8/06 10:02 AM Page 154 154 6 ᭿ THE PSYCHOBIOLOGY OF HUMOR AND LAUGHTER but steady output of research on this topic over the years. The recent publication of several functional magnetic resonance imaging (fMRI) studies (e.g., Azim et al., 2005) as well as articles on topics such as the evolution of humor and laughter (e.g., Gervais and Wilson, 2005) suggest that interest in this topic is increasing (see also Vaid, 2002). As we will see, biological research on humor and laughter highlights the impor- tance of emotional components of humor in addition to the cognitive aspects, point- ing to humor as an interesting topic for investigating the interplay between emotion and cognition more generally. As such, the psychobiological study of humor may be viewed as a subject within the newly developing field of affective neuroscience (Panksepp, 1998). Our discussion of biological aspects of humor also provides an opportunity to focus more closely on many interesting questions concerning the nature and functions of laughter. In this chapter, I will begin by discussing laughter as an emotional display that expresses the positive emotion of mirth, followed by an overview of research on the acoustics, respiration, phonation, and facial expressions of laughter, as well as the autonomic and visceral concomitants of mirth. The subsequent discussion of laughter in nonhuman animals will underscore the close connection between humor, laughter, and play. I will then explore several other laughter-related topics, including patho- logical laughter conditions, laughter and the brain, and tickling as a stimulus for laughter. Next, I will turn to investigations of the brain areas involved in the cognitive and emotional processing of humor, including studies of humor in patients with localized brain damage as well as studies of normal subjects using EEG and fMRI. Finally, I will discuss theories about the evolutionary origins and adaptive functions of humor and laughter. THE NATURE OF LAUGHTER As many authors have noted, boisterous laughter comprises a very strange set of behaviors. A hypothetical alien from outer space would certainly be struck by the oddity of this behavior, noting the loud, barking noises that are emitted, the repeti- tive contractions of the diaphragm and associated changes in respiration, the open mouth and grimaces caused by contractions of facial muscles, the flushing of the skin, increased heart rate and general physiological arousal, production of tears in the eyes, loss of strength in the extremities, and flailing body movements (cf. Askenasy, 1987; Keith-Spiegel, 1972). Such hearty laughter seems to take over the whole organism in an uncontrollable and compulsive way, conveying almost overwhelming feelings of enjoyment and amusement. It is also very contagious and difficult to fake (van Hooff and Preuschoft, 2003). What a peculiar way for people to respond to the perception of humor! Koestler (1964) characterized laughter as a physiological reflex, and suggested that it is the only domain in which a highly complex mental stimulus (i.e., humor) produces such a stereotyped reflexive response. However, as van Hooff and Preuschoft ch006-P372564.qxd 15/8/06 10:02 AM Page 155 THE NATURE OF LAUGHTER 155 (2003) have pointed out, the term reflex is a misnomer because, unlike reflexes, laughter is highly dependent on motivational and emotional states and social context. Instead, laughter seems to be best characterized as a “fixed action pattern,” a ritual- ized and largely stereotyped behavior pattern that serves as a communication signal. Laughter and Emotion As Charles Darwin (1872) noted in The Expression of the Emotions in Man and Animals, laughter is essentially an emotional expression, a way of communicating to others that one is feeling a particular emotion. Thus, laughter is one of many largely hardwired behavior patterns used by humans to communicate a wide range of positive and negative emotions, including various facial expressions (e.g., scowling, frown- ing), vocal sounds (e.g., gasping, screaming), bodily actions (e.g., trembling, shaking the fist), changes in speech patterns (e.g., shouting, whining), and so on. In the case of laughter, the particular emotion that is communicated is a pleasurable feeling closely related to joy. As noted in Chapter 1, researchers have not yet settled on an agreed-upon technical name for this emotion, with different scholars referring to it as “amusement,” “humor appreciation,” or “exhilaration.” I prefer the term mirth, which captures its emotional nature as well as its association with humor and laughter. The emotion of mirth is therefore primary, with laughter (along with smiling) being an emotional display. The more intense the emotion, the stronger the expressive display. At low levels of intensity, mirth is expressed by a faint smile, which turns into a broader smile and then audible chuckling and laughter as the emotional intensity increases. At very high intensity, it is expressed by loud guffaws, often accompa- nied by a reddening of the face as well as bodily movements such as throwing back the head, rocking the body, slapping one’s thighs, and so on. Although, as we will see, there is evidence that smiling and laughter may have different evolutionary origins, they are very closely related in humans, with smiling and laughter occurring along a continuum of emotional intensity. The same facial muscles are involved in laughter and smiling, with stronger contractions of longer duration occurring in laughter than in smiling (Ruch, 1993). The close connection between smiling and laughter is also evident in the fact that laughter typically begins as a smile and, after the laughter ends, gradually fades smoothly back into a smile once again (Pollio, Mers, and Lucchesi, 1972). Like all emotions, mirth has behavioral, physiological, and experiential components. In addition to the vocalizations, facial expressions, and bodily actions that characterize the expressive behavior of laughter, mirth involves a range of physiological changes that take place in the brain, autonomic nervous system, and endocrine system, along with subjective feelings of pleasure, amusement, and cheerfulness. I will discuss each of these components in the following sections. As we will see, the emotion of mirth that is expressed by laughter also appears to be closely related to play. Much of the laughter of early childhood may be seen as an expression of the exuberant ch006-P372564.qxd 15/8/06 10:02 AM Page 156 156 6 ᭿ THE PSYCHOBIOLOGY OF HUMOR AND LAUGHTER delight associated with physical play activities such as running, chasing, and rough- and-tumble play-fighting, as well as incongruous playful actions such as peek-a-boo games. Since social play is an important activity in juveniles of all mammal species, the evolutionary origins of mirth and laughter in play may well extend to our earliest mammalian ancestors some 60 million years ago. As children’s cognitive and linguistic abilities develop, they begin to laugh not only at physical play, but also in response to the sorts of playful manipulation of incongruous ideas, words, and concepts that we call “humor.” Thus, humor may be viewed as a cognitive-linguistic form of play that elicits the emotion of mirth which, in turn, is typically expressed through laughter. Humor may not be the only stimulus that elicits the emotion of mirth and the laughter that expresses it. This emotion may also be elicited by several other stimuli, including nitrous oxide (N2O, or “laughing gas”) and possibly tickling (Niethammer, 1983; Ruch, 1993). At any particular time, an individual’s threshold for experiencing mirth can be raised or lowered by a variety of factors, such as the social context (e.g., feelings of safety, the presence of other people who are laughing), one’s current mood (cheerfulness versus depression; Deckers, 1998; Ruch, 1997), health status, level of fatigue, ingestion of alcohol or psychoactive drugs (Lowe et al., 1997; J. B. Weaver et al., 1985), and more enduring personality traits such as one’s overall sense of humor (Ruch, 1993). Acoustics of Laughter The characteristic that most strikingly distinguishes laughter from other human activities is the loud and distinctive sounds that are emitted.

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