The Physiological Psychology of Humor and Laughter
Abstract
In the first section of this chapter, The Nature of Laughter, we discuss the relationship between laughter and emotion, followed by an overview of research on the facial expressions of laughter and smiling, the acoustics of laughter, and pathological laughter. In the next section, Laughter in Animals, we underscore the close connection between humor, laughter, and play. Then, in the section Where do Humor and Laughter Occur in the Brain?, we address the different areas of the brain that are implicated in the cognitive, emotional, and behavioral (laughter) processes of humor. Finally, we discuss evolutionary psychology theories that attempt to account for the origins and adaptive functions of humor and laughter. Also in this chapter, the brain regions and neural circuits underlying humor, mirth, and laughter are discussed. Recent advancements in fMRI and EEG technology have allowed physiological psychologists to make significant advancements in our understanding of the brain regions responsible for the cognitive processes of humor comprehension. Consistent with cognitive theories of humor (e.g., incongruity theory, comprehension-evaluation theory), studies have shown that incongruity detection and resolution occur in different brain regions. In addition, research using neuroimaging technology has distinguished the neural circuitry and brain regions involved in mirth and consequent laughter from the cognitive processes involved in humor comprehension. In sum, physiological psychology has made considerable progress in advancing our understanding of the underlying brain structures and biochemical processes implicated in humor and laughter.
Keywords
Brain circuits; cognitive; humor; laughter; mirth
Like all psychological phenomena, humor is based on 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/cognitive process draws on systems located in many regions of the cerebral cortex, those involved in visual and auditory perception, language comprehension, social cognition, and logical reasoning. The perception of something as funny stimulates parts of the brain (e.g., prefrontal cortex, limbic system) responsible for producing emotions of mirth and amusement. Such emotions, in turn, stimulate the production and release of biochemical molecules that produce further changes in the brain and body through the autonomic nervous system and endocrine system. In addition, the activation of mirthful emotion typically triggers the expressive behavioral responses of smiling and laughter, which involve the brainstem and its connections to the forebrain, as well as the 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 physiological psychology (also known as psychobiology or biological psychology). Physiological psychologists study the biological underpinnings of behavior and psychological states in brain chemistry and the nervous system. Thus, they attempt to develop and test theories about a variety of psychological phenomena in terms of the brain-behavior relationship (Carlson, 2008). Historically, the study of humor and laughter has not been a major focus in physiological psychology. However, the recent publication of several studies using sophisticated equipment such as fMRI scanners suggests that interest in studying the underlying brain structures and biochemical processes implicated in humor and laughter is increasing. As we will see, physiological research into humor and laughter highlights the interplay between cognitive and emotional processes, thus suggesting that humor and laughter could be fruitful topics for investigating the interplay between emotion and cognition more generally.
In the first section of this chapter, The Nature of Laughter, we discuss the relationship between laughter and emotion, followed by an overview of research on the facial expressions of laughter and smiling, the acoustics of laughter, and pathological laughter. In the next section, Laughter in Animals, we underscore the close connection between humor, laughter, and play. Then, in the section Where do Humor and Laughter Occur in the Brain?, we address the different areas of the brain that are implicated in the cognitive, emotional, and behavioral processes (laughter) of humor. Finally, we discuss evolutionary psychology theories that attempt to account for the origins and adaptive functions of humor and laughter.
The Nature of Laughter
Our discussion of the biological underpinnings of humor provides an opportunity to focus more closely on interesting questions concerning the nature and functions 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 vocalization of loud, barking noises, the repetitive 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 & 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 (2003) pointed out, laughter is not actually a reflex. Unlike reflexes, laughter is highly dependent on motivational and emotional states, and social context. We can define laughter, then, as a ritualized and largely stereotyped vocal act that serves as a communication signal (Provine & Yong, 1991; van Hooff & Preuschoft, 2003). Laughter is closely related to smiling; the difference between them is that they represent a different degree of emotional intensity, rather than qualitatively and affectively different responses to a stimulus (Messinger, Cassel, Acosta, & Cohen, 2008; Ruch, 1994). In fact, the same facial muscles are involved in laughing and smiling, with stronger contractions of longer duration occurring in laughter (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, & Lucchesi, 1972).
Nikopoulos (2017) argued that there are four characteristics of laughter that seem to apply universally:
- 1. Laughter communicates information to others. Nikapoulos argued that laughter evolved primarily to facilitate communication, which explains why we are much more likely to laugh and smile in social situations than when we are alone. It also explains why when we do laugh while alone, we do so in response to stimuli that imitate social interaction, such as while reading a book or watching television (Provine, 2001; Scott, Lavan, Chen, & McGettigan, 2014).
- 2. Laugher is mostly invariable. Although people’s laughs do not all sound identical, we all as human beings share anatomical uniformity that produces a degree of similarity in laughter (i.e., short bursts of sound).
- 3. The content of laughter is highly variable. Laughter reflects one’s subjective perception of a situation. Whether or not a person laughs or smiles in a given situation reveals much about their dispositional qualities (e.g., attitudes, personality) that determine their perceptions.
- 4. Laughter is associated with positivity. Nikapoulos contends that in order for laughter to function as a meaningful social signal, people must, for the most part, consensually understand its affective meaning. Further, laughter signals one’s subjective perception that something is funny. Thus, people, by default, assume that laughter and smiling reflect expressions of positive affect; they deviate from this understanding to the extent they perceive expressions of positive affect (particularly a high level of positive affect) as inappropriate or unlikely in a given situation (e.g., nervous laughter, pathological laughter, laughter elicited by tickling).
Laughter and Emotion
Laughter is one of many largely “hard-wired” behavior patterns people use to express emotion. Through laughter, people express a pleasurable feeling closely related to joy. As noted in Chapter 1, Introduction to the Psychology of Humor, researchers have not settled on an agreed-upon name for this emotion, with different scholars referring to it as “amusement,” “humor appreciation,” or “exhilaration.” We prefer the term “mirth,” which captures its emotional nature as well as its association with humor and laughter.
Like other emotions, mirth triggers a range of physiological changes that take place in the brain, autonomic nervous system, and endocrine (hormone) system (Cacioppo, Berntson, Larsen, Poehlmann, & Ito, 2000), along with subjective feelings of pleasure, amusement, and cheerfulness. Since the 1960s, researchers have investigated mirth-induced physiological changes including heart rate, skin conductance, blood pressure, skin temperature, and muscle tension. Although there have been some inconsistent findings (e.g., Harrison et al., 2000; Hubert & de Jong-Meyer, 1991), the results of these investigations generally indicate that mirth is associated with increased activity of the sympathetic nervous system, the branch of the autonomic nervous system associated with the well-known fight-or-flight response (see McGhee, 1983b, for a review of early research).
In one influential study, Lennart Levi (1965) found that participants who watched a comedy film produced more adrenaline and noradrenaline (measured in urine samples) than those who watched an emotionally neutral nature film, and comparable amounts to participants who watched fear- and anger-evoking films. Other experiments have found mirth-related increases in heart rate, skin conductance, and other variables associated with sympathetic arousal (Averill, 1969; Foster, Webster, & Williamson, 2002; Godkewitsch, 1976; Goldstein, Harman, McGhee, & Karasik, 1975; Hubert & de Jong-Meyer, 1990; Jones & Harris, 1971; Langevin & Day, 1972; Marci, Moran, & Orr, 2004). These effects indicate that humor activates the sympathetic-adrenal-medullary (SAM) system, the well-known “fight-or-flight” response of the sympathetic nervous system, which is also involved in stress-related responses such as fear and anger. In several of these experiments, researchers found positive correlations between the perceived funniness of humor stimuli and the amount of increase in physiological arousal, suggesting that stronger feelings of mirth were related to greater activation of the sympathetic nervous system.
In addition to SAM activation, there is some evidence that extended periods of mirth activate the hypothalamic–pituitary–adrenocortical (HPA) system, the stress response that causes the adrenal cortex to release cortisol into the bloodstream. Hubert and de Jong-Meyer (1990) found that exposure to a brief 9-minute humorous cartoon did not increase salivary cortisol levels. However, Hubert, Moeller, and de Jong-Meyer (1993) found that a longer (90 minutes), and arguably more humorous, Monty Python movie significantly increased cortisol compared to an emotionally neutral nature film. Indeed, 50% of participants who watched the Monty Python movie exhibited HPA activation, as indicated by increased cortisol levels relative to baseline, starting about 1 hour after the beginning of the movie and continuing for 1 hour after it had ended. Hubert et al. also found that the degree to which cortisol increased positively related to participants’ perceptions of the funniness of the movie, indicating that the more amusing participants found the movie, the greater the increase in cortisol they experienced (see Fig. 6.1).
Two findings suggest that the increased physiological arousal in response to humor material is caused by the experience of mirth rather than by laughter per se. First, Foster et al. (2002) found that participants experienced increased heart rate and skin conductance after recalling a humorous experience without actually laughing. Second, the observation that people experience greater physiological changes in response to humor material to the extent they find the material amusing: the stronger the feeling of mirth, the greater the physiological arousal. Thus, laughter does not appear to cause physiological arousal; rather it seems that laughter and peripheral autonomic arousal are separate (although correlated) consequences of mirth.
Overall, it appears that mirth triggers a physiological response of autonomic arousal similar to the “fight-or-flight” response, which prepares the body for vigorous activity. In addition, there is evidence that mirth also causes a loss of muscle tone. Indeed, the expression “weak with laughter” is common to many languages (Overeem, Lammers, & Van Dijk, 1999). With vigorous laughter, people often feel a weakness in their limbs and occasionally even fall to the floor. Supporting this idea, an early study by Paskind (1932) found that participants experienced a decrease in muscle tone in their forearms while they were laughing.
More recently, Sebastiaan Overeem and his colleagues (1999) examined the effects of mirth on the H-reflex, assessed by electrically stimulating a nerve in the leg and using electromyography (EMG) to measure the resultant activation of an adjacent muscle. A severe reduction in amplitude indicates motor inhibition or muscle weakness, such as that seen in cases of cataplexy, in which afflicted individuals suddenly collapse from severe loss of muscle tone. Overeem et al. found that the H-reflex decreased by almost 90% when participants laughed in response to watching humorous slides. In a subsequent study, Overeem, Taal, Gezici, Lammers, and Van Dijk (2004) demonstrated that the emotion of mirth underlying laughter caused this effect, rather than the respiratory or motoric effects of laughter itself. Thus, there appears to be truth to the idea that laughter causes muscle weakness, although, more accurately, it appears that the mirthful emotion underlying laughter causes muscle weakness.
While the positive emotion of mirth triggers the activation of the autonomic nervous system (ANS), physiologists debate over the “emotional specificity” of ANS activity: i.e., whether there are ANS distinctions among different emotions (Levenson, 1992). For instance, in her review of the empirical literature, Lisa Feldman Barrett (2006) concluded that diverse emotions have not consistently revealed differentiated autonomic responses or central nervous system activity. In contrast, other literature reviews and empirical studies have identified unique biomarkers for different emotions (e.g., Christie & Friedman, 2004; Harrison et al., 2000; Kragel & LaBar, 2013; Kreibig, 2010; Stemmler, 2009; Stephens, Christie, & Friedman, 2010). For example, positive emotions, compared to negative emotions, seem to involve a smaller increase in blood pressure and less autonomic activation overall (Cacioppo et al., 2000). Moreover, there appear to be nuanced differences in the physiological underpinnings of positive emotions, such as happiness, joy, and amusement (mirth). For instance, mirth and joy are associated with increased heart rate variability, whereas happiness is associated with decreased heart rate variability. All three emotions involve increased electrodermal activity (the state of sweat glands in the skin, which is an indication of autonomic arousal) and faster breathing. These changes, however, are comparatively greater in mirth than in happiness or joy (Kreibig, 2010).
Some researchers (e.g., Gray, 1994; LeDoux, 1994, 2003) have also pointed out that peripheral changes in the autonomic nervous system and endocrine system may be the wrong place to look for physiological differences among different emotions, since these systems have functions that may be common to many different emotions, such as energy requirements, metabolism, and tissue repair. Instead, they argued that more important differences are likely to be found in the brain systems that underlie different emotions. Therefore, although the somatovisceral changes accompanying mirth may be quite similar to those associated with negative emotions like anger and fear, there are likely important differences in the brain systems underlying these emotions, including the production of biochemical molecules such as neuropeptides, neurotransmitters, and opioids (Panksepp, 1993, 1994). These, in turn, may have different implications for health, such as different effects on the immune system (Kennedy, Glaser, & Kiecolt-Glaser, 1990). We discuss the potential effects of humor and laughter on physical health in Chapter 10, The Health Psychology of Humor: Humor and Physical Health.
Facial Expressions of Laughter and Smiling
Laughter is characterized by a distinctive facial display, which closely resembles smiling. This emotional facial display is one way laughter serves as a communication signal. Paul Ekman and his colleagues at the University of California at San Francisco have conducted extensive research on facial expressions of emotion, including smiling and laughter (Ekman, Davidson, & Friesen, 1990; Ekman & Friesen, 1978; Frank & Ekman, 1993). Although they have identified 18 different types of smiles, Ekman and his colleagues have found only one that is reliably associated with genuine enjoyment or amusement. They have named this smile the Duchenne display, after the French anatomist (Guillaume-Benjamin-Amand Duchenne) who first identified it in 1862. Other types of smiles are associated with feigned amusement (“forced” or “faked” smiles) or negative emotions such as embarrassment or anxiety, or other negative emotions coupled with enjoyment (S. L. Brown & Schwartz, 1980). More recent studies continue to examine perceived levels of genuineness of smiles and facial expressions using large databases of facial expressions (e.g., Dawel et al., 2017). Further, physiological psychologists are developing neuro-computing programs with the goal of recognizing Duchenne or “genuine” smiles as well as people do (Wu et al., 2017).
The Duchenne display involves symmetrical, synchronous, and smooth contractions of both the zygomatic major and the orbicularis oculi muscles of the face (see Fig. 6.2). The zygomatic major is the muscle in the cheeks that pulls the lip corners upwards and backwards, while the orbicularis oculi is the muscle that surrounds each eye socket and causes wrinkling of the skin at the outer sides of the eyes (“crow’s feet”). Although most types of smiles involve contractions of the zygomatic major, only genuine enjoyment smiles involve the contraction of the orbicularis oculi, which is less subject to voluntary control.
The Duchenne display occurs in laughter as well as smiling, although laughter often includes some additional muscles, such as those involved in opening the mouth and lowering the jaw (Ruch & Ekman, 2001). Thus, researchers use the presence or absence of the Duchenne display to determine whether a person is smiling or laughing to express genuine, spontaneous enjoyment or to feign amusement.
Ekman and Friesen (1978) developed the Facial Action Coding System (FACS) to measure the contraction of facial muscles involved in the expression of different emotions. Researchers who study laughter can use FACS to distinguish between Duchenne and non-Duchenne laughter. This is important because only Duchenne laughter expresses genuine enjoyment.
Dacher Keltner and George Bonanno (1997), for instance, interviewed adults whose spouses had died 6 months previously, and FACS-coded participants’ laughter during the interviews. Participants who exhibited more Duchenne laughter also reported experiencing more positive emotions (e.g., happiness, joy) and fewer negative emotions (e.g., anger, distress, guilt). They also reported better social adjustment, a more satisfactory relationship with the deceased spouse, and better relationships with others. Keltner and Bonanno showed muted videos of the interviews to a sample of college students. Students who viewed participants exhibiting more Duchenne laughter reported experiencing more positive emotions themselves, and judged the bereaved participants as healthier and better adjusted. These findings suggest that subtle differences in facial expressions during laughter signal the presence or absence of the Duchenne display, thus communicating different emotional states. Interestingly, a person’s facial expressions during laughter affect the emotions of observers, highlighting the role of laughter as a form of emotional communication. More recent studies support these findings, presenting evidence that Duchenne smiles are implicitly associated with psychological proximity, while non-Duchenne smiles are associated with psychological distance (Bogodistov & Dost, 2017).
Acoustics of Laughter
The characteristic that most strikingly distinguishes laughter from other human activities is the loud and distinctive sounds that a person makes while laughing. These laughter sounds appear to serve two functions: (1) to communicate to others one’s joyful and playful emotional state, and (2) to induce this same emotional state in the listeners (Gervais & Wilson, 2005).
In recent years, researchers have begun to study the acoustics (sound properties) of laughter, using methods commonly developed by ethologists to investigate animal vocalizations such as bird songs. Researchers digitize recordings of human laughter and then use computer-based spectrographic procedures to examine their audio waveforms, frequency patterns, and other acoustical characteristics. The unit of analysis in these studies is usually the series of “ha-ha-ha” sounds that one makes during a single exhalation. Researchers refer to such an episode as a “laughter bout,” and the individual “ha” syllables as “calls” (Bachorowski, Smoski, Owen, & Owren, 2001), “notes” (Provine & Yong, 1991), or “pulses” (Ruch & Ekman, 2001).
Robert Provine and Yvonne Yong (1991), at the University of Maryland, analyzed the acoustical properties of 51 laughter bouts produced by male and female university students and staff members. To obtain recordings of laughter, they approached people in public places with a tape recorder and asked them to “simulate hearty laughter.” Most people found it difficult to laugh on command, and their first attempts were typically strained and artificial, presumably because they were not actually experiencing the emotion of mirth that laughter normally expresses. However, the funniness of the activity itself, along with the clowning and kidding of the experimenters, typically caused the subjects to begin feeling amused and they started laughing spontaneously and naturally. Provine and Yong analyzed these natural and spontaneous bouts of laughter.
Laugh bouts ranged from one to 16 notes or calls with an average of four per bout. Each laugh note began with a protracted voiceless aspirant (i.e., a hissing “h” sound not produced by vibration of the vocal cords). This was followed by a forcefully voiced vowel-like sound with an average duration of about 75 ms. Another voiceless aspirant then followed, with an average duration of about 135 ms, followed by the next voiced vowel sound. Thus, each complete “ha” note was about 210 ms in duration, resulting in about five notes typically emitted per second. Not surprisingly, the fundamental frequency (corresponding to the perceived pitch) of male laughter (averaging 276 Hz) was lower than that of females (502 Hz), reflecting the lower pitch of men’s voices. Each laugh note showed a clear harmonic structure, with numerous secondary frequencies that produced a richly harmonious quality.
Based on their analyses, Provine and Yong emphasized the stereotypical nature of laughter, observing that there was very little variability across people in the overall duration of individual notes. Regardless of the number of notes in each bout of laughter, the duration of each note (onset-to-onset internote interval, or INI) seemed to remain fairly constant, at about 210 ms. However, the voiced segment (“vowel sound”) of each note became slightly shorter from the beginning to the end of a laugh bout, while the intervening unvoiced (“h” sound) segments became correspondingly longer, thus maintaining the same overall duration for each note. They also observed that the amplitude (loudness) of each voiced note segment decreased from the beginning to the end of a bout. Interestingly, when played backwards, a laugh bout sounds quite normal, except for the fact that it becomes progressively louder instead of quieter. This is quite different from human speech, which does not sound at all normal when played backwards.
Because Provine and Yong (1991) conducted their analyses on a relatively small sample of laughs obtained from people who were asked to produce laughter, they may not have captured and analyzed the full range of laughter that occurs naturally in social settings. Consequently, they may have concluded that laughter is more stereotyped and unvarying than is actually true. Accordingly, Jo-Anne Bachorowski and her colleagues (2001) at Vanderbilt University conducted more extensive acoustical analyses of laughter using recordings of 1024 laughter bouts from 97 male and female university students. Bachorowski et al. obtained natural laughter samples by recording participants watching humorous videos in a comfortable laboratory setting, either alone or in same-sex or mixed-sex dyads.
In contrast to the stereotypy of laughter that Provine and Yong (1991) found, Bachorowski et al. (2001) found that participants exhibited a great deal of variability and complexity in the acoustic properties of their laughter. Bachorowski et al. identified several different types of individual laugh calls (notes), including voiced “song-like,” unvoiced “grunt-like,” and unvoiced “snort-like” calls, in addition to “glottal pulses,” and “glottal whistles.”
Several different types of calls often occurred within a single bout of laughter, and there was little consistency within individual participants in the types of calls they produced from one laugh bout to another. However, they did find some sex differences. Women produced significantly more bouts containing voiced, song-like calls, whereas men produced more unvoiced, grunt-like laughs. Men and women did not differ, though, in the frequency of unvoiced snort-like laughs. Although there were no sex differences in the overall number of laugh bouts produced in response to the humorous videos, men exhibited slightly longer bouts with more calls per bout.
On average, laugh bouts were comprised of 3.4 calls per bout, with a total duration of 870 ms, but there was a great deal of variability in these numbers. Laugh bouts typically began with a fairly long call (280 ms duration) followed by a series of shorter calls (lasting 130 ms each). Like Provine and Yong, Bachorowski et al. found that the unvoiced “h”-sound segments between calls tended to be shorter at the beginning of a bout and then became progressively longer toward the end. Analyses of fundamental frequencies of calls also indicated a considerable amount of variability, both between and within individuals. Indeed, the fundamental frequencies were often found to change over the course of an individual call, either rising or falling in pitch. Compared to shorter bouts, longer bouts of laughter tended to have higher mean fundamental frequencies and greater shifts in frequency within calls.
Analyses of the vowel sounds in voiced calls revealed that these are not nearly as distinct or clearly articulated as the vowels of speech, but tend to be a central, unarticulated schwa (like the “a” sound in “about”). Contrary to the observations of Provine and Yong (1991), “ho-ho” and “he-he” laughs were extremely rare, while “ha-ha” was much more common. Nonetheless, there was some evidence that individuals tend to have distinct laughs based on slight variations in the vowel sounds and other vocal characteristics that they produce while laughing. Bachorowski and her colleagues concluded that laughter is much less stereotyped than Provine and Yong (1991) had initially claimed, but rather represents a “repertoire of sounds.” Arguing that laughter has an important social communication function, they suggested that these different sounds of laughter combine in various ways to communicate subtle differences in emotions to other people.
In a series of experiments, Silke Kipper and Dietmar Todt (2001, 2003a, 2003b), at the Free University of Berlin, took a somewhat different approach to studying the acoustics of laughter. Using computer equipment, they systematically modified various acoustical parameters of natural laughter bouts, such as the duration of laugh notes, the fundamental frequencies, and amplitude (loudness). They then had participants listen to these altered laugh bouts and asked them to rate the degree to which these laughs sounded like normal laughter, as well as rating their emotional responses to them. Among a number of interesting findings, these researchers found that laughter can diverge to a considerable degree on various acoustical parameters and still be perceived as normal laughter. Moreover, laugh bouts that showed substantial variability across calls were considered more natural, and elicited more positive emotional responses as compared to more stereotyped bouts containing little variability. These findings cast further doubt on the view of laughter as a highly stereotyped vocalization. Additional findings from these studies supported the view of laughter as a method of communicating positive emotions and eliciting similar emotional responses in others. For example, the more natural-sounding a laugh bout was rated to be, the more it elicited a positive emotional response. More recent research has found further evidence supporting these claims. Lavan, Scott, and McGettigan (2016), for example, found that when presented with authentic laughter and fake laughter, people responded to the acoustic predictors of authentic laughter without needing the verbal cues described in Duchenne laughter (for additional research on acoustics of laughter, see Mowrer, 1994; Mowrer, LaPointe, & Case, 1987; Nwokah, Hsu, Davies, & Fogel, 1999; Vettin & Todt, 2004).
Pathological Laughter
Brain disorders involving pathological laughter are well known in the neurological literature, and practitioners have reported numerous cases since the late 1800s (Duchowny, 1983; Forabosco, 1998; Poeck, 1985). The study of pathological laughter, in connection with knowledge of the underlying brain abnormalities, is one way that neuroscientists have been able to make inferences about the brain sites that may be involved in normal laughter. Pathological laughter differs from natural laughter in that it (1) contains unusual motor patterns, (2) occurs in the absence of pleasant and mirthful emotional experience, or (3) occurs in an inappropriate social context or in the absence of humorous stimuli. Duchowny (1983) distinguished three major categories of pathological laughter, each of which has different clinical manifestations and anatomical substrates: (1) excessive laughter, (2) forced laughter, and (3) gelastic epilepsy.
Excessive Laughter
Excessive laughter conditions involve emotional instability, heightened feelings of mirth and euphoria, an inability to inhibit laughter, and a lack of insight into the abnormality of the laughter. Excessive laughter conditions most commonly occur in adulthood and tend to be associated with disorders such as schizophrenia, mania, and dementia that affect parts of the brain involved in emotion production and regulation, including the limbic system and parts of the frontal lobes.
One such disorder is Angelman syndrome (AS) named after the English physician, Harry Angelman, who first identified the disorder. AS is a neurological disorder that causes severe intellectual/cognitive disability, motor dysfunction, speech impairment, seizures, and hyperactivity. People suffering from AS display gait ataxia (jerky gait), excitability, and an inappropriately happy mood coupled with excessive laughter and smiling (Dagli, Mueller, & Williams, 1998; Williams, 2010). For several decades, the cause of AS remained a mystery (Williams, 2010). However, medical scientists now believe that AS is caused by mutations in the maternal gene, UBE3A (Margolis, Sell, Zbinden, & Bird, 2015).
Forced Laughter
Patients suffering from forced laughter conditions exhibit involuntary outbursts of explosive, self-sustained laughter, often accompanied by autonomic disturbances of heart rate and vasomotor control. Although they may appear to others to be feeling genuinely amused, these patients usually do not subjectively experience the positive emotion of mirth that normally accompanies laughter, but rather experience laughter as unpleasant, embarrassing, and something to be endured. Many forced laughter patients also exhibit pathological crying, with fits of laughter merging into crying or vice versa. Indeed, it can be difficult to tell whether they are laughing or crying. This indicates that some of the brain centers controlling laughter and crying are located very close together (likely in the part of the brainstem called the pons), suggesting a close link between the positive emotions of social play and the distressing emotions associated with social separation (Panksepp, 1998).
Forced laughter conditions typically begin in adulthood and can result from a variety of disorders, including degenerative brain diseases such as Parkinson disease, multiple sclerosis (MS), and amyotrophic lateral sclerosis (ALS), as well as tumors and lesions in various parts of the brain due to cerebrovascular accidents (strokes) and brain injury. Pathological “forced laughter” conditions have been associated with lesions in many areas of the brain, ranging from the frontal and temporal lobes of the cortex and the pyramidal tracts to the ventral mesencephalon, the cerebellum, and the pons (Wild, Rodden, Grodd, & Ruch, 2003; Zeilig, Drubach, Katz-Zeilig, & Karatinos, 1996). In most of these cases, the effect of the lesions seems to be chronic disinhibition of laughter-generating circuitry (i.e., an inability to inhibit or modulate laughter normally), rather than an excitatory effect. People suffering from the condition fou rire prodromique (pathology of crazy laughter) experience uncontrolled laughter lasting up to half an hour or even longer. Such episodes can signal the onset of a stroke in the brainstem. In some tragic cases, people have literally laughed themselves to death.
Gelastic Laughter
The neurological condition gelastic epilepsy, first documented in 1873 (Holmes & Goldman, 2012), causes patients to experience seizures in the form of uncontrolled bouts of laughter. Motor convulsions, eye movement abnormalities, and autonomic disturbances often accompany laughter during seizures. Furthermore, patients typically lose consciousness and report unawareness of these “laughter attacks.” In cases where the patients remain conscious during the seizure, some report a pleasant feeling of mirth, but most experience the laughter as inappropriate and even unpleasant. The laughter typically lasts less than a minute, but can be more prolonged when associated with complex partial seizures (Arroyo et al., 1993). Gelastic epilepsy usually begins in childhood, and cases have even been reported in newborn infants, demonstrating that the neural circuits for laughter are fully developed at birth (Sher & Brown, 1976; see Téllez-Zenteno, Serrano-Almeida, & Moien-Afshari, 2008 for a review).
Brain imaging studies have identified several brain regions that are associated with gelastic seizures, most importantly the hypothalamus, temporal lobes, and medial frontal lobe (Arroyo et al., 1993; Tran et al., 2014). The most common type of gelastic epilepsy, which has also been studied most extensively, is associated with hypothalamic hamartomas, which consist of nonmalignant abnormal tissue growth in the hypothalamus. Indeed, seizures have been best resolved with resection, ablation, or irradiation of the hypothalamic hamartomas (Téllez-Zenteno et al., 2008; Incorpora et al., 2013). Research has shown that the hypothalamus and pituitary gland release hormones during seizures, and it appears that the abnormal hypothalamic electrical activity spreads to areas in the limbic system and brainstem to produce the psychophysiological manifestations of laughter (Wild et al., 2003). These findings suggest that the hypothalamus has an important role in normal laughter. As noted earlier, the hypothalamus functions as a control center for the autonomic arousal associated with the fight-or-flight response, and it regulates a range of motivational states including hunger and sexual arousal (as psychology professors frequently explain to their students, the hypothalamus is responsible for the four “f’s”: feeding, fighting, fleeing, and sexual intercourse).
Laughter in Animals
Although some researchers have suggested that humans are the only animal that laughs (e.g., Stearns, 1972), primatologists have studied in some detail a form of laughter emitted by young chimpanzees and other apes, including bonobos, orangutans, and gorillas (Preuschoft & van Hooff, 1997; van Hooff & Preuschoft, 2003). Primatologists describe ape laughter as a staccato, throaty, panting vocalization that accompanies the relaxed open-mouth display or “play face,” and is emitted during playful rough-and-tumble social activities such as wrestling, tickling, and chasing games. Although it sounds somewhat different from human laughter, it is quite recognizable as such, occurring in similar social contexts.
The “Play Face” and Laughter in Primates
Van Hooff and Preuschoft (2003, p. 267) described the play face depicted in Fig. 6.3 as follows:
The mouth is opened wide and the mouth corners may be slightly retracted. In most (but not all!) primate species the lips are not retracted but still cover the teeth. In many species, this facial posture is often accompanied by a rhythmic staccato shallow breathing (play chuckles) and by vehement but supple body movements. The posture and movements, both of the face and of the body as a whole, lack the tension, rigidity, and brusqueness that is characteristic of expressions of aggression, threat, and fear.
The play face, as the name suggests, occurs while the animals are involved in social play. Play is a common activity among juveniles, not only in primates, but in all mammal species and even some birds. In play, animals perform many activities that are normally important for survival, such as hunting, fighting, mating, fleeing, and simple locomotion (jumping, sliding, pirouetting) “just for fun,” with a great deal of exuberance and energy. Young primates spend many hours in playful mock fighting, chasing, attacking, wrestling, and tickling one another, perhaps as a way of programming various cortical brain functions and developing the social skills needed to perform such behaviors in more “serious” contexts later in life (Gervais & Wilson, 2005; Panksepp, 1998). When primates are playfully fighting and chasing each other, they use the play face, along with the breathy, panting laughter-like grunts, to let each other know that they are just having fun and not seriously intending to harm one another. At the same time, though, researchers recognize that animal play involving the play face can be competitive. Indeed, Panksepp (1998) describes rough-and-tumble play in all mammal species as “joyful social exchange with a strong competitive edge” (p. 284). During bouts of play, animals frequently pin each other down, and one individual often emerges as the more dominant. However, for the playful interactions to continue, the dominant individual must also allow the less dominant one to “win” quite frequently. In much the same way, teasing and other forms of verbal play in humans appear to be ways of competing in a friendly way, and those who tease others are required also to playfully accept the teasing directed at them by others.
Ross, Bard, and Matsuzawa (2014) found that chimpanzees make the play face to signal playful intentions as young as 12 months old. Ross et al. observed that young chimps made the play face more often when engaging in mock fighting than when engaging in “benign play” (i.e., bouncing and acrobatics). Chimpanzees also readily make the play face and “laugh” during playful interactions with human caretakers in zoos. As with human infants, tickling and peek-a-boo games containing an element of surprise, occurring in a relaxed and trusting social atmosphere, are particularly effective at eliciting laughter in chimps.
In their recent research on the facial expressions and play intensity in 10 Western Lowland gorillas, Waller and Cherry (2012) distinguished between two play faces: the “play face” and the “full play face.” Whereas gorillas expressed the play face with an open mouth and only the lower teeth exposed, they expressed the full play face with an open mouth and both the upper and lower teeth exposed. Waller and Cherry coded how often gorillas made each face while engaging in gentle play (i.e., tickling, play biting) and intense play (i.e., chasing a playmate, jumping on playmate with their feet). They found that gorillas made the full play most often while engaging in intense play (80% of the observed full play faces occurred during intense play; only 51% of the standard play faces occurred during intense play). In addition, gorillas engaged in intense play longer when they exhibited the full play face (median = 50.64 seconds) compared to when they exhibited no playful facial expression (median = 13.14 seconds). These findings suggest that gorillas use the full play face when engaging in rough-and-tumble play to communicate playful, rather than aggressive, intentions.
It is interesting to note that, by means of the play face, animals demonstrate an ability to distinguish between reality and pretense, seriousness and play, which, as we have seen in previous chapters, is arguably the essence of humor. Thus, one can make the case that animals exhibit and experience a rudimentary form of humor in addition to laughter. Moreover, chimpanzees and gorillas that have been taught to communicate with sign language have used sign language in playful ways (e.g., making puns, making humorous insults, and using incongruous words) raising the possibility that they have a rudimentary sense of humor (see Gamble, 2001, for a review). Importantly, the apes’ humorous use of sign language is typically accompanied by the play face, providing further evidence for the close connection between linguistic humor and play.
As noted earlier, chimpanzees exhibit “laughter” that is characterized by a staccato, guttural, throaty panting sound associated with rapid and shallow breathing, that typically accompanies the relaxed open-mouth play face display. Other primates such as gorillas, orangutans, and macaques exhibit a similar vocalization (van Hooff & Preuschoft, 2003). Davila-Ross, Allcock, Thomas, and Bard (2011) examined two distinct forms of laughter in chimpanzees, specifically laughter replications (“laughing after the laughter of others”) and spontaneous laughter. In addition to establishing that the laughter replications are directly caused by the laughter of the playmate, they found that play involving laughter replications lasted longer than play involving spontaneous laughter, which lasted longer than play without laughter.
A major difference between human and chimpanzee laughter is that chimpanzees exhibit a unique breathing pattern characterized by a rapid alternation between shallow inhalations and exhalations, with single sounds being produced during each inhalation and exhalation. In contrast, as described previously, human laughter involves a series of multiple “ha-ha-ha” sounds or calls occurring during a single exhalation, with no vocalization during the intervening inhalations.
“Laughter” in Rats?
Physiological psychologist Jaak Panksepp and his colleagues at Bowling Green State University (Burgdorf, Panksepp, & Moskal, 2011; Panksepp, 2000; Panksepp & Burgdorf, 2000, 2003) have provided intriguing evidence that a form of laughter may even exist in rats. They found that laboratory rats produce a high-frequency (approximately 50 kHz), ultrasonic chirping sound during social rough-and-tumble play, and also when being tickled by human handlers. Although humans are unable to hear these sounds without the aid of specialized sound equipment, they are within the auditory range in which rats communicate.
Rats seem to be most ticklish on the nape of the neck, although they also apparently enjoy a “full body” tickle. When they have previously been tickled by a human hand, they will eagerly approach that hand rather than one that has merely petted them, chirping all the while. Like laughter among people, rat “laughter” appears to be contagious, and young rats generally prefer to spend time with older animals that produce more of this chirping sound as compared to those that do not. This chirping “laughter” is also readily conditioned using both classical and operant methods, and animals will run mazes and press levers for an opportunity to be tickled and “laugh.” Rat “laughter” can easily be amplified or reduced by selective genetic breeding, indicating that it reflects a heritable emotional trait.
Finally, Buck, Malavar, George, Koob, and Vendruscolo (2014) examined chirping “laughter” in alcohol-dependent rats. They first conditioned rats to learn the consequence of pressing two levers: one was responsible for dispensing alcohol, the other water. Then, they exposed some rats to alcohol vapor to create a group of alcohol-dependent (alcoholic) rats. They exposed the nonalcohol-dependent rats to air only. Next, they placed the rats in the experimental chamber with the levers retracted for two minutes and measured anticipatory chirping laughter. Finally, they left the rats in the chamber for 30 minutes to “self-administer” alcohol or water by pressing the respective levers. Buck et al. found a positive correlation between the frequency of “laughing” among dependent rats in the 2-minute anticipatory period and their amount of alcohol intake during the 30-minute reinforcement session. In other words, the alcoholic rats that drank more in the reinforcement session “laughed” more in anticipation.
Panksepp and Burgdorf (2003) suggested that this chirping “laughter” arises from organized “ludic” (from Greek ludos = play) brain circuits that form the “emotional operating system” for the positive emotion of joy (or what we call mirth), which is activated during social play, and which may be common to all mammals. They postulated that play-related joy has an important social facilitation and bonding function in mammals, promoting cooperative forms of social engagement and helping to organize social dynamics. They suggested that rough-and-tumble play in rats, accompanied by chirping “laughter,” may provide a useful animal model for researchers to investigate the brain structures mediating positive emotions relating to play and laughter, in much the same way that other animal models have been used to elucidate the brain mechanisms of negative emotions such as fear and anger (Panksepp, 1998). Research using this model has already begun to shed light on the neural bases of positive playful emotion. For example, this research suggests an important role of endorphins and other opioids, the morphine-like substances created in certain brain sites. Low doses of morphine increase play in rats, whereas the opiate antagonist naloxone (which inhibits the effect of opioids) decreases play (Panksepp, 1998). These findings suggest that opioid systems may also be involved in mirthful humor and laughter in humans.
Where Does Humor Occur in the Brain?
Based on evidence from cases of pathological laughter and electrical brain stimulation, and from animal studies, electroencephalogram (EEG) studies, and functional magnetic resonance imaging (fMRI) studies, neuroscientists are piecing together the regions and circuits of the brain that control the cognitive, emotional, and motor processes involved in humor. As with other emotional systems (Panksepp, 1998), the structures and circuits underlying humor and laughter are distributed throughout the brain, including regions in the neocortex, basal ganglia, diencephalon, limbic system, and brain stem. In this section, we provide a brief overview of research attempting to identify the different areas of the brain that are implicated in the cognitive processes, emotional experience, and behavioral expression (laughter) of humor.
Cognitive Processes of Humor
Cases involving electrical brain stimulation suggest the cognitive processes of humor can be isolated in different parts of the brain from emotional and motor processes. Surgeons commonly electrically stimulate various areas of the exposed surface of the brain when patients undergo brain surgery for treatment of epileptic seizures in order to localize areas that should and should not be removed. The patients remain conscious during this procedure. These electrical probes occasionally trigger laughter in the patients, with or without accompanying feelings of mirth. Fried and colleagues (1998), for instance, described an epileptic patient who consistently laughed whenever surgeons stimulated a small region of the supplementary motor area located on the left frontal lobe of the cortex of her brain. Interestingly, she attributed her laughter (caused by electrical stimulation) to various stimuli in her environment and reported feeling amused. For example, she would say that she laughed because of the funny appearance of a picture of a horse that she happened to be looking at, or because the people in the room behaved in an amusing way. It appears that when surgeons induced mirthful feelings through electric stimulation, the patient’s brain generated cognitive-perceptual incongruities to account for them.
Overall, this remarkable case provides evidence that cognitive processes of humor can be dissociated from the emotional and motor components of mirth and laughter. Other research designed to more explicitly delineate the brain structures and circuitry underlying the cognitive processes involved in humor have focused on (1) distinguishing the roles of structures in the right versus left hemispheres of the brain, and then more recently on (2) identifying specific structures that are responsible for detecting and resolving incongruity.
Right Hemisphere Versus Left Hemisphere
Clinical observations of patients with right hemisphere damage (RHD) resulting from strokes or other brain injury have suggested that the right hemisphere plays an important role in the processing of humor material. Although RHD patients typically have normal linguistic abilities, they often fail to “get a joke” or understand the main point of a story. Interestingly, they can understand elements of a joke or details of a story, but cannot piece them together to form a coherent interpretation. In addition, they have difficulty extracting inferences and nuances from communication, and consequently misunderstand sarcasm (Brownell & Gardner, 1988).
In contrast, patients with left hemisphere damage (LHD) often suffer aphasia (they exhibit language impairment because language functions are located in the left hemisphere in right-handed people). However, to the extent allowed by their linguistic impairments, they usually can combine elements of a joke or story into a coherent whole in order to get the joke or understand the story. In sum, the comparison of RHD and LHD patients suggests that RHD patients have difficulty understanding and appreciating at least some forms of humor.
In one study, Bihrle, Brownell, and Powelson (1986) compared the ability of RHD and LHD patients to comprehend humor. Bihrle et al. selected a series of captionless comic strips, each containing four picture panels forming a narrative, with the final picture introducing a humorous ending much like the punch line of a verbal joke. They presented participants with the first three panels from the comic strips and instructed them to select from two alternative pictures that would make the funniest ending. In each case, one alternative was the original picture that contained an incongruity that made sense with the rest of the comic strip (incongruity + resolution). One of the other alternatives contained an incongruous ending that did not make sense or follow from the first three panels of the comic strip (incongruity without resolution); the other contained a nonsurprising coherent ending (resolution without incongruity). By examining which “wrong” (less funny) alternatives participants chose, Bihrle et al. could identify which part of humor comprehension (incongruity detection or incongruity resolution) gave them difficulties.
Bihrle et al. made two interesting discoveries. First, they found that RHD patients had more difficulty selecting the correct alternative, indicating that the right hemisphere plays an important role in humor comprehension. Second, RHD patients were particularly likely to select incongruous endings that did not follow from the first three panels of the comic strip (incongruity without resolution). For example, instead of the correct, funny ending, they would often select a slap-stick ending (e.g., a picture of someone slipping on a banana peel) that was completely irrelevant to the rest of the comic strip. Thus, they seemed to be aware that humor involves some sort of incongruity, and were able to recognize (detect) incongruity, but had difficulty identifying which incongruous endings made sense in relation to the rest of the comic strip. This inability to recognize relevance or coherence might account for the clinical observation that RHD patients often engage in silly, socially inappropriate forms of humor (i.e., humor that is not relevant to the social situation). Interestingly, when LHD patients made errors, they were more likely than RHD patients to choose incorrect endings that did not contain any incongruity, but simply provided an ordinary, unsurprising completion to the story. Thus, LHD patients showed some difficulty recognizing incongruity.
Other researchers found similar results using different stimuli, including verbal jokes rather than visual cartoons (e.g., Brownell, Michel, Powelson, & Gardner, 1983; Wapner, Hamby, & Gardner, 1981). Overall, it appears that the left hemisphere of the brain plays a role in perceiving incongruity, whereas the right hemisphere is important for making coherent sense of (i.e., resolving) the incongruity within the social context (Bihrle, Brownell, & Gardner, 1988; Gillikin & Derks, 1991; McGhee, 1983b).
More recent research suggests that part of the difficulty of RHD patients in comprehending humor involves deficits in “theory of mind”—the ability to attribute beliefs and intentions to other people in order to explain or predict their behavior (Brownell & Stringfellow, 2000). Francesca Happé, Hiram Brownell, and Ellen Winner (1999) tested humor comprehension in groups of RHD and LHD patients and non-brain-damaged control participants using nonverbal cartoons that either did or did not require a sophisticated theory of mind in order to understand and appreciate the humor. In the theory of mind cartoons, the humor depended on what a character mistakenly thought or did not know. For example, in one cartoon a man was playing a guitar and singing on a balcony of a high-rise apartment building, while two women, one on the balcony above him and the other on the balcony below, were listening with rapt attention, each apparently thinking that he was serenading her. To understand the joke, one must be able to recognize differences in the beliefs and perceptions of each of the characters.
Happé et al. presented participants with pairs of cartoons, each comprised of the original humorous cartoon and a modified version in which the key humorous element had been replaced with something less funny. Participants were asked to choose which of the two cartoons was funnier. RHD patients exhibited more errors than both the LHD patients and the normal control participants in identifying the humorous cartoons that involved theory of mind, but not in identifying the humorous cartoons that did not involve theory of mind. In contrast, LHD patients did not differ from non-brain-damaged participants in identifying the humorous option for either type of cartoon.
Brownell and Stringfellow (2000) suggested the inability to attribute beliefs and intentions to other people accounts for the difficulty RHD patients have shown in resolving or “making sense” of incongruity. They proposed that incongruity resolution often depends on theory of mind—correctly attributing beliefs and intentions to other people. Also, it is noteworthy that appropriate social and emotional functioning also involves theory of mind. Thus, impairments in theory of mind could account for the socially inappropriate forms of humor RHD patients often exhibit (see also Lyons & Fitzgerald, 2004, for a discussion of humor in autism and Asperger syndrome, which are thought to involve deficits in theory of mind).
Although previous research indicated an important role of the right hemisphere in humor comprehension, Prathiba Shammi and Donald Stuss (1999), at the University of Toronto, indicated that it is the right frontal lobe, specifically, that seems to be most important. They tested patients with single focal brain damage restricted to the frontal (right, left, or bilateral) or nonfrontal (right or left) brain regions, as well as age-matched normal controls. They gave participants several humor tests to assess the ability to recognize incongruity and incongruity resolution in both verbal and nonverbal forms of humor. Only RHD patients with right frontal lobe damage exhibited similar deficits in incongruity resolution as reported in previous research. Furthermore, they reacted with less emotional responsiveness (smiling and laughter) to all the humorous materials as compared to those with lesions in other brain areas.
Shammi et al. noted that the frontal lobes, and particularly the right frontal lobe, appear to be especially involved in the integration of cognition and emotion, due to their connections to the limbic system, as well as many other cortical regions. In addition to the integration of cognition and emotion, the frontal lobes have been shown to play a crucial role in a number of cognitive functions that are likely important for humor comprehension, including narrative discourse, abstract and nonliteral interpretation, working memory, problem-solving, and indirect forms of communication such as irony, affective intonation, and sarcasm.
To determine whether the left or right hemisphere is more active in humor, Svebak (1982) used an electroencephalogram (EEG) to measure the electrical activity (i.e., the amount of discordant alpha wave activity) occurring at sites on the right and left occipital lobes of healthy participants while they watched a comedy film. He found that participants that laughed while watching the film (and therefore presumably found it highly amusing) showed less discordant right–left alpha activity than did those who did not laugh, suggesting coordinated activity of both hemispheres during mirth. Svebak (1982) conducted a follow-up study in which he replicated these results and demonstrated that the greater concordance in alpha activity across the hemispheres associated with laughter was not simply caused by laughter-related changes in respiration. Overall, then, it appears that the left and right hemispheres of the brain work together in a coordinated manner during humor and mirth, rather than one hemisphere being more active than the other (Box 6.1).
Box 6.1
Advanced technology for studying humor in the brain
Advances in technology have presented a new frontier for physiological psychology research. The first of the three most commonly used technologies is the electroencephalogram (EEG). The EEG detects electrical activity in the brain using electrodes (pictured below). Brain cells constantly communicate by electric impulses (even while you sleep!). EEG recordings help us understand the type of activity taking place when participants are presented with different stimuli (such as a joke).
The electromyography (EMG) test records the zygomatic muscle of the face (the muscle that pulls the corners of the mouth up to form a Duchenne smile), thus detecting the presence or absence of smiling and laughter.
fMRI uses high-powered, rapidly oscillating magnetic fields to scan the brain and detect small changes in blood oxygenation levels (which are indicative of changes in neuronal activity) in specific regions of the brain. Several recent studies have employed this method to investigate humor. These investigations have begun to map out the areas in the cortex involved in the comprehension of humor, as well as subcortical areas in the limbic system underlying the emotional response of mirth.
Specific Brain Structures Responsible for Detecting and Resolving Incongruity
As mentioned in Chapter 2, Classic Theories of Humor, and Chapter 3, Contemporary Theories of Humor, cognitive theories of humor appreciation suggest that humor comprehension involves complex processes of detecting and resolving incongruity. Recent studies using fMRI and EEG technology have lent support to that idea by localizing the specific neural underpinnings of incongruity detection and resolution (e.g., Bekinschtein, Davis, Rodd, & Owen, 2011; Campbell et al., 2015; Chan et al., 2012, 2013; Samson et al., 2008; Shibata, Terasawa, & Umeda, 2014). For instance, Samson et al. (2008) presented participants with visual cartoons that contained resolvable incongruity (incongruity resolution cartoons) or cartoons that contained only an incongruity with no resolution (incongruity only cartoons). Both types of cartoons implicate cognitive processes of incongruity detection, but only the incongruity resolution cartoons involve processes of incongruity resolution. Thus, the areas of the brain uniquely involved in the processing of the incongruity resolution cartoons can be attributed to resolution of incongruity. Results indicated that the processing of the incongruity resolution cartoons involved greater activation of the inferior frontal gyrus (IFG) and the temporoparietal junctions (TPJ) than the processing of incongruity only cartoons. Thus, it appears that the IFG and TPJ are involved in the resolution, but not detection, of incongruity in visual cartoons (see also Wild et al. 2006). These areas appear to play a key role in the semantic integration of complex visual stimuli.
Chan et al. (2013) also found that detection and resolution of incongruities in verbal humor involve different areas of the brain. Chan et al. (2013) presented participants with three types of verbal stimuli: jokes containing resolvable incongruity (incongruity resolution jokes), jokes containing irresolvable incongruity (incongruity only jokes), and nonhumorous stories (no incongruity stories) serving as a baseline or control condition. They placed participants in an fMRI scanner and presented them with 64 jokes or nonhumorous stories. The setup was shown for 20 seconds and the punch line (ending) for 9 seconds. Participants pressed a button on a keypad to indicate that the joke/story was comprehensible or incomprehensible.
The fMRI images of participants exposed to incongruity only jokes showed greater activation in the right middle temporal gyrus (MTG) and the right medial frontal gyrus (MFG) compared to participants in the no incongruity stories control condition. These findings suggest that the right MTG and the right MFG are involved in the process of detecting incongruity. They also found that the brain images for participants exposed to incongruity resolution jokes showed greater activation of the left inferior frontal gyrus (IFG), superior frontal gyrus (SFG), and the left inferior parietal lobule (IPL) compared to participants exposed to incongruity only jokes, indicating that these areas are uniquely involved in the integration of verbal information that is required to resolve incongruities (see Shibata et al., 2014, for similar findings). Fig. 6.4 provides a summary of the brain structures that Chan et al. (2013) and others have found to be involved in incongruity detection and resolution.
Amir, Biederman, Wang, and Xu (2013) extended the investigation of the neural underpinnings of incongruity detection and resolution by comparing the brain regions involved in the detection of humorous versus nonhumorous incongruity. As depicted in Table 6.1, they presented participants with ambiguous drawings followed by captions that provided a:
Table 6.1
Drawing i adopted from “A normative set of 98 pairs of nonsensical pictures (droodles),” by T. Nishimoto et al., 2010, Behavior Research Methods, 42, p. 685. Copyright 2010 by Springer. Reprinted with permission. Drawing ii adopted from “Droodles – The Classic Collection” by Roger Price ©2000 by Tallfellow Press, www.Tallfellow.com. Used by permission. All rights reserved.
So that participants could fully interpret the captions in relation to the drawings, each drawing appeared alone on a screen for two seconds; the caption then appeared for five seconds, followed by the drawing alone again for three seconds. Using neuroimaging software, Amir et al. found many neurological similarities in the processing of the captions that involved humorous and nonhumorous incongruity. Importantly, however, the processing of humorous incongruity uniquely involved several brain regions. Specifically, the captions involving humorous incongruity (but not those that involved nonhumorous incongruity) stimulated the:
The TPs and TOJs play a role in connecting separate concepts, but subsequent activation in the mPFC (reward center) occurred with humorous incongruity. Thus, an interesting implication of these results is that processing humorous incongruity is intrinsically rewarding; processing nonhumorous incongruity involves similar processes, but without the intrinsic reward.
Taken together, recent studies using fMRI and EEG technology have made significant advancements in our understanding of the specific brain regions responsible for the cognitive processing of humor comprehension. These studies are consistent with cognitive theories of humor (discussed in Chapter 2: Classic Theories of Humor and Chapter 3: Contemporary Theories of Humor), which propose that comprehension involves separate processes of incongruity detection and resolution.
Mirth: Emotional Experience of Humor
Studies using EEG and neuroimaging technology have distinguished the neural circuitry and brain regions involved in mirth or amusement (the emotional experience of humor) from the cognitive processes involved in humor comprehension. In one important study, for instance, Peter Derks and colleagues at the National Aeronautics and Space Administration (Derks, Gillikin, Bartolome-Rull, & Bogart, 1997) used an EEG test to examine event-related potentials (ERPs) associated with joke comprehension and appreciation (mirth). ERPs are spikes in positively or negatively polarized brain wave activity occurring at very brief intervals after an event, and appear to indicate different types of information processing. Derks et al. monitored 21 EEG electrodes placed on different spots on participants’ scalps to monitor brain wave activity while they read a series of verbal jokes on a computer screen. Derks et al. also collected EMG recordings of the zygomatic muscle of the face to assess the extent to which participants smiled or laughed at the jokes, thus reflecting the degree to which they experienced mirth or amusement in response to the jokes.
Participants exhibited an increased positive polarization of brain waves with peak amplitude about 300 ms (P300) following presentation of the punch line, regardless of whether or not they smiled or laughed (i.e., regardless of whether or not they experienced mirth). Critically, though, participants also subsequently exhibited a negative polarization with peak amplitude at about 400 ms (N400) only in response to jokes that made them smile or laugh (i.e., jokes that elicited mirth), suggesting that the N400 wave is uniquely associated with mirth apart from humor comprehension (see also Coulson & Kutas, 2001; Marinkovic et al., 2011).
Campbell et al. (2015) also distinguished the neural underpinnings of humor appreciation (i.e., mirth) from comprehension. They placed 24 participants individually in an MRI chamber and showed them 120 comics that were: (1) funny, (2) not funny (but intended to be funny), or (3) altered and not intended to be funny. Campbell used neuroimaging software to measure blood oxygen level dependent (BOLD) neural responses to each stimulus. To identify the regions involved in humor comprehension, they examined BOLD responses that were unique to the funny comics relative to the comics that were not funny but intended to be funny. They found that humor comprehension was associated with BOLD responses in the inferior frontal gyrus (IFG), bilateral temporal pole gyrus (TP), and bilateral temporoparietal junction (TPJ). They identified regions involved in humor appreciation by comparing BOLD responses unique to the funny comics relative to the ones that were not intended to be funny. Humor appreciation (mirth) was associated with BOLD responses in the bilateral substantia nigra (SN) and bilateral amygdala. Osaka, Yaoi, Minamoto, and Osaka (2014) reported similar findings in a study of humor appreciation of Manga comics.
A number of other studies found similar patterns of activation in subcortical brain regions in response to humorous stimuli (e.g., Azim, Mobbs, Jo, Menon, & Reiss, 2005; Mobbs, Greicius, Abdel-Azim, Menon, & Reiss, 2003; Mobbs et al., 2005; Shibata et al., 2014). For instance, Mobbs et al. (2003) found that participants exhibited greater activation in the following regions comprising the mesolimbic reward network in response to humorous versus nonhumorous cartoons (see Fig. 6.5):
Laughter: The Behavioral Expression of Humor
Physiologists believe that the activation of the emotion induction centers that produce mirth stimulates emotion effector (expression) sites, including the motor and premotor areas of the cerebral cortex (initiating facial and bodily movements), the hypothalamus (controlling autonomic responses such as increased heartrate and flushing), thalamus, periaqueductal gray matter, reticular formation, cranial nerve nuclei (controlling facial, laryngeal, and respiratory actions), and parts of the brainstem, all of which are involved in smiling and laughter as the expression of mirth. Most authors agree that there is likely a final common pathway for laughter located in the brainstem (possibly in the dorsal area of the pons) which coordinates the respiratory, laryngeal, and facial components of laughter (Wild et al., 2003).
In addition to excitatory input triggering laughter, inhibitory signals arriving in the brainstem from various higher centers in the brain serve to inhibit inappropriate laughter. Most researchers believe that the pathological laughter described earlier is due to damage involving the corticobulbar tract, a motor pathway originating in the frontal cortex and terminating in cranial motor nuclei in the pons and medulla, which results in a failure of these laughter inhibition mechanisms (Mendez, Nakawatase, & Brown, 1999). Parvizi and colleagues (2001) have also hypothesized a possible role of the cerebellum in modulating the intensity and duration of laughter. According to this view, the cerebellum receives information concerning the current social-emotional context from the cortex and telencephalic structures, and feeds this information back to various effector sites.
In this way, laughter may be inhibited or amplified, depending on its appropriateness to the social and emotional situation (e.g., whether one is at a party or a funeral). However, when a stroke or other disease causes lesions to specific regions of the cerebellum or to the relevant structures and pathways leading into or out of it, this modulation does not take place, resulting in pathological laughter occurring in socially and emotionally inappropriate contexts (Parvizi, Anderson, Martin, Damasio, & Damasio, 2001).
Recent neuroimaging studies have attempted to more definitively identify the brain regions responsible for laughter. However, because of constraints inherent in fMRI procedures, studies have largely focused on mapping the neurological networks activated when participants observe others laughing (Caruana et al., 2015). The brain regions that appear to be involved in the perception of laughter include temporal areas (basal temporal gyrus, superior temporal gyrus), and the amygdala (e.g., Fusar-Poli et al., 2009; Hennenlotter et al., 2005). As Caruana et al. (2015) noted, some studies on the perception of laughter also reported activation of frontal regions of the brain when participants mimicked the facial expressions of those they observed laughing. Thus, researchers hypothesized that the frontal areas are involved in the motor production of laughter, but not in the cognitive processing of humor stimuli (Hennenlotter et al., 2005).
However, laughter without mirth resulting from tickling activates the temporal gyrus, whereas genuine laughter involving mirth initiated by humorous incongruity or the recall of humorous memories, activates the pregenual anterior cingulate cortex (pACC; Szameitat et al., 2010). Importantly, the ACC connects to emotion induction sites located in the limbic system involved in “turning on” the emotion of mirth, and to the cognitive processing centers in the prefrontal cortex (Stevens, Hurley, & Taber, 2011). This suggests that the pACC could be involved in the cognitive and affective processes of humor, as well as the motor production of laughter. In sum, although further research is needed to clarify the exact brain sites and pathways involved, it is clear that humor is a complex activity involving cognition, emotion, and motor behavior that involves the coordinated activation of a wide range of brain regions, including parts of the cerebral cortex, the limbic system, and the brainstem (Box 6.2).
Box 6.2
A conversation with Dr. Yu-Chen Chan
Authors: When did you first become interested in humor as a topic for psychological inquiry? What was it about humor that you found appealing as a topic of study?
Yu-Chen Chan: My research interests focused mainly on creativity and problem solving before 2007. After that, I started to get interested in humor psychology. Previous behavioral studies of humor showed ample evidence of ratings on comprehension and appreciation of different joke types. By using garden path sentences and nonsensical ones as experimental stimuli innovatively, I further distinguished neural correlates of humor comprehension and affective processes effectively from the perspective of cognitive neuroscience (Chan et al., 2012, 2013).
Authors: What would you say have been the most important developments in the physiological study of humor that you have seen over the course of your career?
Yu-Chen Chan: Humor is an important cognitive and affective phenomenon. Remarkable advances in fMRI techniques have made it possible to study the neural correlates of humor processing. Goel and Dolan (2001)’s study was the earliest to separate cognitive and affective components of humor. Mobbs et al. (2003) proposed that mesolimbic reward centers, as affective components of humor, also play a key role in humor appreciation. Follow-up research also investigated cognitive and affective processes of humor across different humor types (e.g., Bekinschtein et al., 2011; Chan & Lavallee, 2015; Samson et al., 2008). The importance of individual differences in humor processing should not be neglected, such as sex/gender (Azim et al., 2005; Chan, 2016; Kohn, Kellermann, Gur, Schneider, & Habel, 2011) and gelotophobics (Chan, 2016, Scientific Reports).
Authors: In what ways would you say theory and research on the physiology of humor has contributed to the study of humor in other areas of psychology?
Yu-Chen Chan: The tri-component theory of humor (Chan, 2016) I proposed states that humor processes include not only cognition (comprehension) and affect (appreciation), but also laughter (expression). They can be validated by cognitive neuroscience and further applied to explain the differences in humor appreciation and laughter responses between men and women, providing a reference in evolutionary psychology. The distinct processes in humor comprehension, appreciation, and expression (laughter) between men and women could also benefit industrial and organizational psychology, such as the application in advertisement marketing and persuasion. Finally, based on Martin et al.’s (2013) theory of humor styles and Ruch and Proyer’s (2011) theory of gelotophobia and personality traits, gelotophobics’ humorlessness towards hostile jokes (Chan, 2016, Scientific Reports) is examined through cognitive neuroscience, which can contribute to counseling or clinical psychology.
Authors: What do you see as the most significant challenges that physiological psychologists studying humor will have to address in future research?
Yu-Chen Chan: To date, the physiological psychology of humor mostly focuses on general populations; however, it is worth studying special population groups, such as people with autism, gelotophobia, or depression, by contrasting their performance before and after humor training. In addition, more delicate experimental designs can be adopted to investigate the relations between humor and other topics. For example, if humor, monetary, and erotic motivation are all used as rewards, are emotions elicited by these rewards taken in charge by different brain regions? Moreover, previous studies argued that schizophrenia patients with anhedonia symptoms show in-the-moment emotion responses, with the deficit in motivation of anticipation. Researchers can contrast humor and other types of stimuli that can motivate rewards in different anticipatory ways. Finally, although it takes longer to read stimuli for humor (e.g., verbal jokes or cartoons), future studies of humor in neuroscience can still focus on EEG/ERP or EMG techniques, which have better temporal resolutions, to supplement fMRI results showing good spatial resolutions.
Authors: What’s your favorite joke?
Yu-Chen Chan: I like jokes related to life and in which one can seek pleasure from bitterness:
Three brothers live together on the 50th floor of a skyscraper. One day, the elevator is broken so they have to climb the stairs home. On the way upstairs, the elder brother suggests to tell a tragic story by turns. The elder brother starts, and the second brother continues. When it comes to the youngest brother, they are already on the 46th floor. The elder brother says: “Come on, we will be home when you finish it.” The youngest brother says: “Well…but I left the key at home.”
And also jokes illustrating the Piagetian concept of conservation:
On New Year's Eve, Jason wants to have a pizza and watch TV at home while waiting for the New Year's arrival. He goes to the store to order a big one. The clerk asks him: “Sir, do you want the pizza cut into 4 or 8 pieces?” Jason says: “4 pieces. How could I finish 8 pieces?”
Evolutionary Psychology of Humor and Laughter
According to Leda Cosmides and John Tooby at the Center for Evolutionary Psychology, evolutionary psychology is “an approach to psychology, in which knowledge and principles from evolutionary biology are put to use in research on the structure of the human mind. It is not an area of study, like vision, reasoning, or social behavior. It is a way of thinking about psychology that can be applied to any topic within it” (http://www.cep.ucsb.edu/primer.html).
Evolutionary psychology is based on the following underlying assumptions:
- 1. Psychological characteristics (e.g., personality traits) and mechanisms (e.g., working memory) that underlie behavior are adaptations to environmental conditions that increase the odds of survival and reproduction.
- 2. Natural selection is the process that shapes the development of psychological characteristics and mechanisms in response to environmental conditions or barriers to reproduction (Balliet, Tybur, & Van Lange, 2017; Bowlby, 1969; Tooby & Cosmides, 1990, 2005).
The aim of research in evolutionary psychology is to explain the origins and functions of psychological characteristics and mechanisms that underlie behavior from the framework of Darwin’s theory of evolution (1859) and theory of sexual selection (1871) by identifying how those characteristics and mechanisms function as adaptions to environmental barriers to reproduction (Box 6.3).
Evolutionary psychologists studying humor attempt to explain how humor (in particular, humor production and humor appreciation) affords a survival benefit (e.g., Gervais & Wilson, 2005; Weisfeld, 1993). Geoffrey Miller’s theory of mental fitness indicators (Miller, 1998, 2000, 2007) offers one explanation. Miller’s theory is rooted in Darwin’s (1871) sexual selection theory, and thus proposes that certain traits and behaviors (e.g., creativity, intelligence, music ability, humor) characteristics have a reproductive advantage, not because they directly confer a survival advantage, but because they increase one’s ability to attract a mate. Such traits require complex cognitive functions that resist mutations; thus, they signal good mental fitness and good genetic make-up. Accordingly, from this framework, humor (particularly humor production) is a sexually selected trait that evolved through natural selection because it signals intelligence and thus good genes (Bressler & Balshine, 2006; Bressler, Martin, & Balshine, 2006; Kaufman, Kozbelt, Bromley, & Miller, 2008).
Sexual selection theories hold that women have a greater investment in parenting than men do, making them particularly attuned to signals of cognitive competence (e.g., Trivers, 1972). From this perspective, women should prefer men who display cognitive competence, and thus should prefer men who have greater humor ability over those that do not (Bressler et al., 2006; Wilbur & Campbell, 2011). Consistent with Miller’s sexual selection theory, research shows that in the context of courtship or mate selection, women often do, indeed, favor men with good humor ability as potential partners for a serious relationship or marriage (e.g., Bressler et al., 2006; Lundy, Tan, & Cunningham, 1998). Eric Bressler and Sigal Balshine (2006), for instance, presented male and female undergraduates photographs of two “target” people (both either male or female) along with statements that were supposedly written by them. The statements from one of each pair always contained humor and the other did not. Participants rated the targets on a number of perceived personality traits and selected the target that was most desirable as a relationship partner. Bressler and Balshine found that women preferred the humorous male target over the nonhumorous male target as a potential relationship partner; men exhibited no preference for either the humorous or nonhumorous female target.
Other research, however, has produced findings that are not consistent with the sexual selection hypothesis. Li et al. (2009), for instance, found that both men and women (not just men) expected to use humor when interacting with an attractive potential romantic partner or someone with whom they already had an on-going relationship. Furthermore, both men and women (not just women) judged a funny opposite sex person as more attractive than a nonfunny person. Finally, when watching videos of speed dating interactions, both men and women perceived humor production and appreciation among both male and female partners as a signal of romantic interest. Based on these findings, it appears that both men and women try to be funny to invoke interpersonal attraction from others, and both men and women are attuned to humor production in potential romantic partners.
Also, research has shown mixed results for the hypothesized mechanism that humor signals intelligence. Supporting the hypothesized sexual selection mechanism, Greengross and Miller (2011) found that general and verbal intelligence both positively correlated with humor production ability, which in turn predicted “mating success” (number of sexual partners). They also found that men exhibited better humor ability than women. Greengross and Miller contend that these findings indicate that “the human sense of humor evolved at least partly through sexual selection as an intelligence-indicator” (p. 188). Other research, however, has failed to support the sexual selection hypothesis that humor is an honest indicator of intelligence. Indeed, Lundy et al. found that women perceived humorous men as less intelligent (but more cheerful) than nonhumorous men. Similarly, Senko and Fyffe (2010) asked women to give their impressions of men using “pick-up” lines that were either humorous or nonhumorous. Participants preferred men for a long-term relationship who used nonhumorous pick-up lines because the humorous ones conveyed lower intelligence, among other things. In addition, Hall (2015) asked participants to rate a number of “target” people along various dimensions after reading their Facebook profiles. Hall found that participants rated targets as more extraverted, but not more intelligent, to the extent their Facebook profiles were funny.
Finally, in a review of the relevant literature, Robert Storey (2003) concluded that humor “may have evolved as an instrument for achieving broad social adhesiveness and for facilitating the individual’s maneuverability within the group, but that it evolved through sexual selection has yet to be convincingly demonstrated” (p. 319). On the basis of these equivocal findings and new empirical findings, Li et al. (2009) suggested that people do not use humor as a basis for mate selection as proposed by an evolutionary psychology perspective, but rather to implicitly communicate their interest in another person, whether romantic or platonic (p. 925). Li et al. thus propose that people use humor as a strategy to initiate and monitor interpersonal relationships of all kinds.
Summary and Conclusion
Physiological psychology is the study of the biological underpinnings of behavior and psychological states in brain chemistry and the nervous system. From a physiological perspective, we first considered the nature of laughter and its connection to the emotion, mirth. Mirth seems to trigger a physiological response of autonomic arousal similar to the “fight-or-flight” response, and the expressive behavior of smiling and laughing. Paul Ekman and his colleagues identified the Duchenne display, occurring in smiling and laughter, as reflecting genuine, spontaneous mirth. Laughter involves a distinctive pattern of vocalizations and a fixed action pattern that serves an interpersonal communication function. It has a contagious effect, as the sound of laughter elicits feelings of mirth in others, causing them to laugh as well.
Interestingly, laughter is not a uniquely human phenomenon. Primatologists have found that chimpanzees and other apes, including bonobos, orangutans, and gorillas all exhibit a form of laughter. Primatologists describe ape laughter as a staccato, throaty, panting vocalization that accompanies the relaxed open-mouth or “play face,” and is emitted during playful rough-and-tumble social activities such as wrestling, tickling, and chasing games, highlighting the close connection between humor, laughter, and play.
In this chapter, we also discussed the brain regions and neural circuits underlying humor, mirth, and laughter. Recent advancements in fMRI and EEG technology have allowed physiological psychologists to make significant advancements in our understanding of the brain regions responsible for the cognitive processes of humor comprehension. Consistent with cognitive theories of humor (e.g., incongruity theory, comprehension-evaluation theory), studies have shown that incongruity detection and resolution occur in different brain regions. In addition, research using neuroimaging technology has distinguished the neural circuitry and brain regions involved in mirth and consequent laughter from the cognitive processes involved in humor comprehension. In sum, physiological psychology has made considerable progress in advancing our understanding of the underlying brain structures and biochemical processes implicated in humor and laughter.
Finally, the physiological approach draws attention to evolutionary psychology theories of humor. Evolutionary psychologists studying humor attempt to explain how humor affords a survival benefit. For instance, Geoffrey Miller’s theory of mental fitness indicators proposes that humor production ability, among other traits and behaviors, has a reproductive advantage, not because it directly confers a survival advantage, but because it increases one’s ability to attract a mate. Specifically, humor production requires complex cognitive functions and thus signals good mental fitness and good genetic make-up. Accordingly, from this framework, humor (particularly humor production) is a sexually selected trait that evolved through natural selection because it signals intelligence and thus good genes.
Key Concepts
- • Mirth
- • Sympathetic–adrenal–medullary system
- • Hypothalamic–pituitary–adrenocortical system
- • Cataplexy
- • Duchenne display
- • Zygomatic major
- • Orbicularis oculi
- • Excessive laughter
- • Forced laughter
- • Gelastic epilepsy
- • Angelman syndrome
- • Fou rire prodromique
- • Ape laughter
- • Cognitive processes of humor
- • Aphasia
- • Right frontal lobe
- • Electroencephalogram (EEG)
- • Electromyography (EMG)
- • Functional magnetic resonance imaging (fMRI)
- • Blood oxygen level dependent
- • Mesolimbic reward network
- • Hypothalamus
- • Thalamus
- • Periaqueductal gray matter
- • Reticular formation
- • Cranial nerve nuclei
- • Brainstem
- • Corticobulbar tract
- • Frontal cortex
- • Cranial motor nuclei
- • Pons
- • Medulla
- • Cerebellum
- • Temporal areas
- • Amygdala
- • Temporal gyrus
- • Pregenual anterior cingulate cortex
- • Prefrontal cortex
Critical Thinking
- 1. Consider the opening cartoon: the characters state that “nothing is funny” and that they are just “having a good laugh.” What behavior might you see in these characters engaging in laughter without the possible presence of mirth? What brain function may or may not occur in this situation? If they were truly experiencing mirth, how might their behavior and brain functions differ?
- 2. In viewing humorous incongruity and nonhumorous incongruity images, participants in Amir et al.’s (2013) study only showed activation of the mPFC in the humorous incongruity condition, indicating pleasure at “getting” the joke. However, how might this compare to more complicated nonhumorous incongruities, such as riddles? Would you expect similar or dissimilar effects? Design a study in which you examine the impact of humorous (jokes) and nonhumorous incongruities (riddles) on study participants. Include hypothesis, conditions, measures, participants, and expected results.
- 3. Much of the research discussed in this chapter focuses on incongruity resolution through the presentation of canned jokes and cartoons. How might other forms of humor differentiate themselves in terms of brain processes? How might these different forms of humor impact the experience of mirth? What other factors might impact the physiology of humor differently?
- 4. This chapter discusses humor from an evolutionary psychological perspective. Does this perspective adequately explain the adaptation of humor behavior in humans? Why or why not? Are there other evolutionary explanations, besides sexual selection, that may account for the use of humor?