Biopsychology of Emotion, Stress, and Health PDF

Chapter 17 Biopsychology of Emotion, Stress, and Health Fear, the Dark Side of Emotion fizkes/Shutterstock Chapter Overview and Learning Objectives Biopsychology of Emotion: LO 17.1 S...

Chapter 17 Biopsychology of Emotion, Stress, and Health Fear, the Dark Side of Emotion fizkes/Shutterstock Chapter Overview and Learning Objectives Biopsychology of Emotion: LO 17.1 Summarize the major events in the history of research on Introduction the biopsychology of emotion. LO 17.2 Summarize the research on the relationship between the ­autonomic nervous system and emotions. LO 17.3 Describe some research on the facial expression of emotions. Fear, Defense, and LO 17.4 Describe the work that led to the distinction between Aggression ­aggressive and defensive behaviors in mammals. LO 17.5 Describe the relation between testosterone levels and ­aggression in males. 461 M17_PINE1933_11_GE_C17.indd 461 22/01/2021 11:47  462 Chapter 17 Neural Mechanisms of Fear LO 17.6 Describe the role of the amygdala in fear conditioning. Conditioning LO 17.7 Describe the role of the hippocampus in contextual fear conditioning. LO 17.8 Describe the role of two specific amygdalar nuclei in fear conditioning. Brain Mechanisms of LO 17.9 Describe the current status of cognitive neuroscience research Human Emotion on emotion. LO 17.10 Describe the role of the amygdala in human emotion. LO 17.11 Describe the role of the medial prefrontal lobes in human emotion. LO 17.12 Describe the research on the lateralization of emotion. LO 17.13 Describe the current perspective on the neural mechanisms of human emotion that has emerged from brain-imaging studies. Stress and Health LO 17.14 Describe the components of the stress response. LO 17.15 Describe research on animal models of stress, including that on subordination stress. LO 17.16 Describe how our view of psychosomatic disorders has been refined by the results of research on gastric ulcers. LO 17.17 Define psychoneuroimmunology, and describe the four ­components that make up our bodies’ defenses against foreign pathogens. LO 17.18 Describe the effects of early exposure to severe stress. LO 17.19 Describe the effects of stress on the hippocampus. This chapter is about the biopsychology of emotion, stress, Early Landmarks in the and health. It begins with a historical introduction to the biopsychology of emotion and then focuses in the next two Biopsychological Investigation modules on the dark end of the emotional spectrum: fear. of Emotion ­Biopsychological research on emotions has concentrated LO 17.1 Summarize the major events in the history of on fear not because biopsychologists are a scary bunch, but research on the biopsychology of emotion. because fear has three important qualities: It is the easiest emotion to infer from behavior in various species; it plays an This section describes, in chronological sequence, six early important adaptive function in motivating the avoidance of landmarks in the biopsychological investigation of emotion. threatening situations; and chronic fear is one common source It begins with the 1848 case of Phineas Gage. of stress. In the final two modules of the chapter, you will learn how some brain structures have been implicated in human emotion, and how stress increases susceptibility to illness. The Mind-Blowing Case of Phineas Gage Biopsychology of Emotion: In 1848, Phineas Gage, a 25-year-old construction foreman for the Rutland and Burlington Railroad, was the victim of a tragic Introduction accident. In order to lay new tracks, the terrain had to be lev- eled, and Gage was in charge of the blasting. His task involved To introduce the biopsychology of emotion, this module drilling holes in the rock, pouring some gunpowder into each reviews several classic early discoveries and then discusses hole, covering it with sand, and tamping the material down with the role of the autonomic nervous system in emotional a large tamping iron before detonating it with a fuse. On the experience and the facial expression of emotion. fateful day, the gunpowder exploded while Gage was tamping M17_PINE1933_11_GE_C17.indd 462 22/01/2021 11:47  Biopsychology of Emotion, Stress, and Health 463 interspecies comparisons, Darwin developed a theory of the it, launching the 3-cm-thick, 90-cm-long tamping iron through his face, skull, and brain and out the other side. evolution of emotional expression that was composed of Amazingly, Gage survived his accident, but he survived it a three main ideas: changed man. Before the accident, Gage had been a responsi- Expressions of emotion evolve from behaviors that ble, intelligent, socially well-adapted person, who was well liked indicate what an animal is likely to do next. by his friends and fellow workers. Once recovered, he appeared to be as able-bodied and intellectually capable as before, but his If the signals provided by such behaviors benefit the personality and emotional life had totally changed. Formerly a animal that displays them, they will evolve in ways that religious, respectful, reliable man, Gage became irreverent and enhance their communicative function, and their origi- impulsive. In particular, his abundant profanity offended many. nal function may be lost. He became so unreliable and undependable that he soon lost Opposite messages are often signaled by opposite his job, and was never again able to hold a responsible position. movements and postures, an idea called the principle Gage became itinerant, roaming the country for a dozen of antithesis. years until his death in San Francisco. His bizarre acci- dent and apparently successful recovery made headlines Consider how Darwin’s theory accounts for the evo- around the world, but his death went largely unnoticed and lution of threat displays. Originally, facing one’s enemies, unacknowledged. rising up, and exposing one’s weapons were the com- Gage was buried next to the offending tamping iron. Five ponents of the early stages of combat. But once enemies years later, neurologist John Harlow was granted permission began to recognize these behaviors as signals of impend- from Gage’s family to exhume the body and tamping iron to ing aggression, a survival advantage accrued to attackers study them. Since then, Gage’s skull and the tamping iron have that could communicate their aggression most effectively been on display in the Warren Anatomical Medical Museum at Harvard University. and intimidate their victims without actually fighting. As a result, elaborate threat displays evolved, and actual combat declined. To be most effective, signals of aggression and submis- In 1994, Damasio and her colleagues brought the sion must be clearly distinguishable; thus, they tended to power of computerized reconstruction to bear on Gage’s evolve in opposite directions. For example, gulls signal classic case. They began by taking an x-ray of the skull aggression by pointing their beaks at one another and sub- and measuring it precisely, paying particular attention mission by pointing their beaks away from one another; to the position of the entry and exit holes. From these primates signal aggression by staring and submission by measurements, they reconstructed the acci- dent and determined the likely region of Gage’s brain damage (see Figure 17.1). It Figure 17.1 A reconstruction of the brain injury of Phineas Gage. The was apparent that the damage to Gage’s damage focused on the medial prefrontal lobes. brain affected both medial prefrontal lobes, which we now know are involved in plan- ning, decision making, and emotion (see Jin & Maren, 2015; Lee & Seo, 2016; Simon, Wood & Moghaddam, 2015). DARWIN’S THEORY OF THE EVOLUTION OF EMOTION. The first major event in the study of the biopsychology of emotion was the publication in 1872 of Darwin’s book The Expression of Emotions in Man and Animals. In it, Darwin argued that particular emotional responses, such as human facial expressions, tend to accompany the same emotional states in all members of a species. Darwin believed that expressions of emo- tion, like other behaviors, are products of evolution; he therefore tried to understand them by comparing them in different spe- cies (see Brecht & Freiwald, 2012). From such Patrick Landmann/Science Source M17_PINE1933_11_GE_C17.indd 463 22/01/2021 11:47  464 Chapter 17 averting their gaze. Figure 17.2 reproduces the woodcuts usual commonsense way of thinking about the causal Darwin used in his 1872 book to illustrate this principle of relation between the experience of emotion and its antithesis in dogs. expression (see Figure 17.3). James and Lange argued that the autonomic activity and behavior that are trig- JAMES-LANGE AND CANNON-BARD THEORIES. The gered by the emotional event (e.g., rapid heartbeat and first physiological theory of emotion was proposed inde- running away) produce the feeling of emotion, not vice pendently by James and Lange in 1884. According to the versa (see Figure 17.3). James-Lange theory, emotion-inducing sensory stimuli Around 1915, Cannon proposed an alternative to the are received and interpreted by the cortex, which triggers James-Lange theory of emotion, and it was subsequently changes in the visceral organs via the autonomic nervous extended and promoted by Bard. According to the system and in the skeletal muscles via the somatic ner- ­Cannon-Bard theory, emotional stimuli have two inde- vous system. Then, the autonomic and somatic responses pendent excitatory effects: They excite both the ­feeling trigger the experience of emotion in the brain. In effect, of emotion in the brain and the expression of emotion what the James-Lange theory did was to reverse the in the autonomic and somatic nervous systems. That is, the ­Cannon-Bard theory, in contrast to the James-Lange ­theory, views emotional experience and emotional expres- sion as parallel processes that have no direct causal Figure 17.2 Two woodcuts from Darwin’s 1872 book, relation. The Expression of Emotions in Man and Animals, that he used to illustrate the principle of antithesis. The aggressive The James-Lange and Cannon-Bard theories make dif- posture of dogs features ears forward, back up, hair up, ferent predictions about the role of feedback from auto- and tail up; the submissive posture features ears back, nomic and somatic nervous system activity in emotional back down, hair down, and tail down. experience. According to the James-Lange theory, emo- tional experience depends entirely on feedback from auto- nomic and somatic nervous system activity; according to the Cannon-Bard theory, emotional experience is totally independent of such feedback. Both extreme positions have proved to be incorrect. On the one hand, it seems that the autonomic and somatic feedback is not necessary for the experience of emotion: Human patients whose auto- nomic and somatic feedback has been largely eliminated by a broken neck are capable of a full range of emotional experiences, though there does seem to be some dampen- ing of fear and anger (see Pistoia et al., 2015). On the other hand, there have been numerous reports—some of which you will soon encounter—that autonomic and somatic Aggression responses to emotional stimuli can influence emotional experience. Failure to find unqualified support for either the James-Lange or the Cannon-Bard theory led to the modern biopsychological view. According to this view, each of the three principal factors in an emotional response—the per- ception of the emotion-inducing stimulus, the autonomic and somatic responses to the stimulus, and the experience of the emotion—can influence the other two (e.g., Scherer & Moors, 2019; see Figure 17.3). SHAM RAGE. In the late 1920s, Bard (1929) discov- ered that decorticate cats—cats whose cortex has been removed—respond aggressively to the slightest provoca- tion: After a light touch, they arch their backs, erect their hair, hiss, and expose their teeth. Submission The aggressive responses of decorticate animals are abnormal in two respects: They are inappropriately severe, M17_PINE1933_11_GE_C17.indd 464 22/01/2021 11:47  Biopsychology of Emotion, Stress, and Health 465 is critical for the expression of aggres- Figure 17.3 Four ways of thinking about the relations among the ­perception of emotion-inducing stimuli, the autonomic and somatic responses to the sive responses and that the function of ­stimuli, and the emotional experience. the cortex is to inhibit and direct these responses. LIMBIC SYSTEM AND EMOTION. In Perception of bear 1937, Papez (pronounced “Payps”) proposed that emotional expression is controlled by several interconnected nuclei and tracts that ring the thalamus. Feeling of fear Figure 17.4 illustrates some of the key structures in this circuit: the amygdala, mammillary body, hippocampus, fornix, cingulate cortex, septum, olfactory bulb, Physiological and hypothalamus. Papez proposed that reactions emotional states are expressed through Commonsense View the action of the other structures of the circuit on the hypothalamus and that they are experienced through their action on Perception the cortex. Papez’s theory of emotion was of bear revised and expanded by Paul MacLean in 1952 and became the influential limbic Perception of bear system theory of emotion. Indeed, many Physiological of the structures in Papez’s circuit are reactions part of what is now known as the limbic ­system (see Figure 3.27). Feeling Feeling Physiological KLÜVER-BUCY SYNDROME. In 1939, of fear of fear reactions Klüver and Bucy observed a striking syn- drome (pattern of behavior) in monkeys James-Lange View Cannon-Bard View whose anterior temporal lobes had been removed. This syndrome, which is com- monly referred to as the Klüver-Bucy Perception ­syndrome, includes the following behav- of bear iors: the consumption of almost anything that is edible, increased sexual activity often directed at inappropriate objects, a tendency to repeatedly investigate familiar objects, Feeling Physiological of fear reactions a tendency to investigate objects with the mouth, and a lack of fear. ­Monkeys that could not be handled before surgery were Modern Biopsychological View transformed by bilateral anterior temporal lobectomy into tame subjects that showed no fear ­whatsoever—even in response to snakes, which terrify normal monkeys. In and they are not directed at particular targets. Bard referred primates, most of the symptoms of the Klüver-Bucy syndrome to the exaggerated, poorly directed aggressive responses of have been attributed to damage to the a­ mygdala (see LeDoux, decorticate animals as sham rage. Michel, & Lau, 2020; Schröder, Moser, & H ­ uggenberger, Sham rage can be elicited in cats whose cerebral 2020), a structure that has played a major role in research on hemispheres have been removed down to, but not ­emotion, as you will learn later in this chapter. including, the hypothalamus; but it cannot be elicited The Klüver-Bucy syndrome has been observed in sev- if the hypothalamus is also removed. On the basis of eral species. Following is a description of the syndrome in this observation, Bard concluded that the hypothalamus a human patient with a brain infection. M17_PINE1933_11_GE_C17.indd 465 22/01/2021 11:47  466 Chapter 17 Figure 17.4 The location of the structures that Papez Emotions and the Autonomic proposed controlled emotional expression. Nervous System Cingulate LO 17.2 Summarize the research on the relationship cortex between the autonomic nervous system and Septum Fornix emotions. Research on the role of the autonomic nervous system (ANS) in emotion has focused on two issues: the degree to which specific patterns of ANS activity are associated with specific emotions and the effectiveness of ANS measures in polygraphy (lie detection). EMOTIONAL SPECIFICITY OF THE AUTONOMIC ­NERVOUS SYSTEM. The James-Lange and Cannon-Bard theories differ in their views of the emotional specificity of Olfactory the autonomic nervous system. The James-Lange ­theory bulb says that different emotional stimuli induce different pat- Hypothalamus terns of ANS activity and that these different patterns produce different emotional experiences. In contrast, the Amygdala Mammillary Cannon-Bard theory claims that all emotional stimuli pro- body Hippocampus duce the same general pattern of sympathetic activation, which prepares the organism for action (i.e., increased heart rate, increased blood pressure, pupil dilation, increased flow of blood to the muscles, increased respiration, and A Human Case of Klüver-Bucy increased release of epinephrine and norepinephrine from Syndrome the adrenal medulla). The experimental evidence suggests that the specific- At first he was listless, but eventually he became very placid ity of ANS reactions lies somewhere between the extremes with flat affect. He reacted little to people or to other aspects of of total specificity and total generality (see Kreibig, 2010; his environment. He spent much time staring at the television, ­Quigley & Barrett, 2014). On one hand, ample evidence even when it was not turned on. On occasion he would become indicates that not all emotions are associated with the same extremely silly, smiling inappropriately and mimicking the actions of others, and once he began copying the movements of pattern of ANS activity; on the other, there is no evidence another person, he would persist for extended periods of time. that each emotion is characterized by a distinct pattern of In addition, he tended to engage in oral exploration, sucking, ANS activity (see Siegel et al., 2018). licking, or chewing all small objects that he could reach. POLYGRAPHY. Polygraphy (more commonly known as the “lie detector test”) is a method of interrogation that employs ANS indexes of emotion to infer the truth- The six early landmarks in the study of brain mecha- fulness of a person’s responses. Polygraph tests admin- nisms of emotion just reviewed are listed in Table 17.1. istered by skilled examiners can be useful additions to normal interrogation procedures, but they are far from infallible. The main problem in evaluating the effectiveness of Table 17.1 Biopsychological Investigation of Emotion: polygraphy is that it is rarely possible in real-life situations Six Early Landmarks to know for certain whether a suspect is guilty or innocent. Event Date Consequently, many studies of polygraphy have employed Case of Phineas Gage 1848 the mock-crime procedure: Volunteers participate in a mock crime and are then subjected to a polygraph test by an Darwin’s theory of the evolution of emotion 1872 examiner who is unaware of their “guilt” or ­“innocence.” James-Lange and Cannon-Bard theories about 1900 The usual interrogation method is the control-question Discovery of sham rage 1929 technique, in which the physiological response to the Discovery of Klüver-Bucy syndrome 1939 target question (e.g., “Did you steal that purse?”) is com- Limbic system theory of emotion 1952 pared with the physiological responses to control questions M17_PINE1933_11_GE_C17.indd 466 22/01/2021 11:47  Biopsychology of Emotion, Stress, and Health 467 whose answers are known (e.g., “Have you ever been in to open their eyes wide so as to reveal white above the iris, jail before?”). The assumption is that lying will be associ- to slacken the muscles around their mouth, and to drop ated with greater sympathetic activation. A review of the their jaw. Try it. use of the control-question technique in real-life crime set- tings led to an estimated success rate of about 55 ­percent— UNIVERSALITY OF FACIAL EXPRESSION. Several early just slightly better than chance (i.e., 50%) (see Iacono & studies found that people of different cultures make similar ­Ben-Shakhar, 2019). facial expressions in similar situations and that they can cor- Despite being commonly referred to as lie detection, rectly identify the emotional significance of facial expres- polygraphy detects ANS activity, not lies. Consequently, it sions displayed by people from cultures other than their is less likely to successfully identify lies in real life than in own. The most convincing of these studies was a study of experiments. In real-life situations, questions such as “Did the members of an isolated New Guinea tribe who had had you steal that purse?” are likely to elicit an emotional reac- little or no contact with the outside world (see Ekman & tion from all suspects, regardless of their guilt or innocence, Friesen, 1971). making it difficult to detect deception (see Ambach & Gamer, 2018). The guilty-knowledge technique, also PRIMARY FACIAL EXPRESSIONS. Ekman and Friesen known as the concealed information test, circumvents this concluded that the facial expressions of the following six problem. In order to use this technique, the polygrapher emotions are primary: surprise, anger, sadness, disgust, must have a piece of information concerning the crime that fear, and happiness. They further concluded that all other would be known only to the guilty person. Rather than facial expressions of genuine emotion are composed of mix- attempting to catch the suspect in a lie, the polygrapher tures of these six primaries. Figure 17.5 illustrates these six simply assesses the suspect’s reaction to a list of actual and primary facial expressions. contrived details of the crime. Innocent suspects, because they have no knowledge of the crime, react to all such FACIAL FEEDBACK HYPOTHESIS. Is there any truth to details in the same way; the guilty react differentially (see the old idea that putting on a happy face can make you feel Ambach & Gamer, 2018). better? Research suggests that there is. The hypothesis that In the classic study of the guilty-knowledge technique our facial expressions influence our emotional experience is (Lykken, 1959), volunteers waited until the occupant of an called the facial feedback hypothesis. In a test of the facial office went to the washroom. Then, they entered her office, feedback hypothesis, Rutledge and Hupka (1985) instructed stole her purse from her desk, removed the money, and left volunteers to assume one of two patterns of facial contrac- the purse in a locker. The critical part of the interrogation tions while they viewed a series of slides; the patterns cor- went something like this: “Where do you think we found responded to happy or angry faces, although the volunteers the purse? In the washroom?... In a locker?... Hanging were unaware of that. They reported that the slides made on a coat rack? ” Even though electrodermal activity was them feel more happy and less angry when they were mak- the only measure of ANS activity used in this study, 88 ing happy faces and less happy and more angry when they percent of the mock criminals were correctly identified; were making angry faces (see Figure 17.6). A recent meta- more importantly, none of the innocent control volunteers analysis of the facial feedback hypothesis confirmed the was judged guilty—see Ben-Shakhar (2012), Ambach & reliability of these and similar findings; however, the effects Gamer (2018). were smaller than originally believed (see Coles, Larsen, & Lench, 2019). Emotions and Facial Expression LO 17.3 Describe some research on the facial expression of emotions. Check It Out Ekman and his colleagues have been preeminent in the study of facial expression (see Ekman, 2016). They began Experiencing Facial Feedback in the 1960s by analyzing hundreds of films and photo- Why don’t you try the facial feedback hypothesis? Pull your graphs of people experiencing various real emotions. eyebrows down and together; raise your upper eyelids and From these, they compiled an atlas of the facial expres- tighten your lower eyelids, and narrow your lips and press sions that are normally associated with different emo- them together. Now, hold this expression for a few seconds. tions (Ekman & Friesen, 1975). For example, to produce If it makes you feel slightly angry and uncomfortable, you the facial expression for surprise, models were instructed have just experienced the effect of facial feedback. to pull their brows upward so as to wrinkle their forehead, M17_PINE1933_11_GE_C17.indd 467 22/01/2021 11:47  468 Chapter 17 Figure 17.5 Ekman’s six primary facial expressions of emotion. Katerina Solovyeva/123RF to substitute false ones. There are many reasons for choos- Figure 17.6 The effects of facial expression on the ­experience of emotion. Participants reported feeling more ing to put on a false facial expression. Some of them are happy and less angry when they viewed slides while ­making positive (e.g., putting on a false smile to reassure a worried a happy face and less happy and more angry when they friend), and some are negative (e.g., putting on a false viewed slides while making an angry face. smile to disguise a lie). In either case, it is difficult to fool an expert. Happiness-inducing Anger-inducing There are two ways of distinguishing true expressions slides slides from false ones (Ekman, 1985). First, microexpressions (brief Degree of Emotion The effect of facial facial expressions) of the real emotion often break through expression on the the false one (see Wang et al., 2015). Such microexpressions experience of emotion last only about 0.05 second, but with practice they can be detected without the aid of slow-motion photography. ­Second, there are often subtle differences between genuine facial expressions and false ones that can be detected by skilled observers. The most widely studied difference between a genu- Happy Angry Happy Angry ine and a false facial expression was first described by the Facial Expression Facial Expression French anatomist Duchenne in 1862. Duchenne said that the smile of enjoyment could be distinguished from delib- Based on Rutledge, L. L., & Hupka, R. B. (1985). The facial feedback ­hypothesis: Methodological concerns and new supporting evidence. ­Motivation and ­Emotion, erately produced smiles by consideration of the two facial 9, 219–240. muscles that are contracted during genuine smiles: orbicu- laris oculi, which encircles the eye and pulls the skin from the cheeks and forehead toward the eyeball, and zygomati- VOLUNTARY CONTROL OF FACIAL EXPRESSION. cus major, which pulls the lip corners up (see Figure 17.7). Because we can exert voluntary control over our facial According to Duchenne, the zygomaticus major can be con- muscles, it is possible to inhibit true facial expressions and trolled voluntarily, whereas the orbicularis oculi is normally M17_PINE1933_11_GE_C17.indd 468 22/01/2021 11:47  Biopsychology of Emotion, Stress, and Health 469 Figure 17.7 A fake smile. The orbicularis oculi and the Figure 17.8 An expression of pride. zygomaticus major are two muscles that contract during genuine (Duchenne) smiles. Because the lateral portion of the orbicularis oculi is difficult for most people to contract vol- untarily, fake smiles usually lack this component. This young woman is faking a smile for the camera. Look at her eyes. Steven J. Barnes contracted only by genuine pleasure. Thus, inertia of the Reproduced with permission of Jessica Tracy, Department of Psychology, orbicularis oculi in smiling unmasks a false friend—a fact University of British Columbia. you would do well to remember. Ekman named the genuine smile the Duchenne smile. FACIAL EXPRESSIONS: CURRENT PERSPECTIVES. Fear, Defense, and Ekman’s work on facial expressions began before video recording became commonplace. Now, video recordings Aggression provide almost unlimited access to natural facial expres- Most biopsychological research on emotion has focused on sions made in response to real-life situations. This tech- fear and defensive behaviors. Fear is the emotional reaction nology has contributed to four important qualifications to to threat; it is the motivating force for defensive behaviors. Ekman’s original theory. First, it is now clear that Ekman’s Defensive behaviors are behaviors whose primary function six primary facial expressions of emotion rarely occur in is to protect the organism from threat or harm. In contrast, pure form—they are ideals with many subtle variations. aggressive behaviors are behaviors whose primary func- Second, the existence of other primary emotions has been tion is to threaten or harm. recognized (see Whalen et al., 2013). Third, body cues, not Although one purpose of this module is to discuss just facial expressions, are known to play a major role in fear, defense, and aggression, it has another important expressions of emotion (see Sznycer, 2019). For example, purpose: to explain a common problem faced by bio- pride is expressed through a small smile, with the head psychologists and the way in which those who conduct tilted back slightly and the hands on the hips, raised research in this particular area have managed to circum- above the head, or clenched in fists with the arms crossed vent it. Barrett (2006) pointed out that progress in the on the chest—see Figure 17.8 (see Witkower & Tracy, study of the neural basis of emotion has been limited 2019). Fourth, there is evidence that Ekman’s six primary because neuroscientists have often been guided by unsub- facial expressions may not be as universal as originally stantiated cultural assumptions about emotion: Because believed. For example, there seem to be distinct differ- we have words such as fear, happiness, and anger in our ences, in terms of both the expression and recognition of language, scientists have often assumed that these emo- facial expressions, between Western Caucasian and East tions exist as entities in the brain, and they have searched Asian individuals (see Calvo & Nummenmaa, 2015; Jack for them—often with little success. The following lines of et al., 2012; Wood et al., 2016). Moreover, recent studies research on fear, defense, and aggression illustrate how of isolated tribes by Crivelli et al. (2016, 2017) indicate that biopsychologists can overcome the problem of vague, sub- facial expressions of emotion are not as universal as once jective, everyday concepts by basing their search for neu- thought. ral mechanisms on the thorough descriptions of relevant M17_PINE1933_11_GE_C17.indd 469 22/01/2021 11:48  470 Chapter 17 behaviors, the environments in which they occur, and the sequences led to two important conclusions. The first con- putative adaptive functions of such behaviors (see Kasai clusion was that, in contrast to the common belief, cats do et al., 2015; LeDoux & Hofmann, 2018). not play with their prey; the cats that appeared to be play- ing with the mice were simply vacillating between attack and defense. The second conclusion was that one can best Journal Prompt 17.1 understand each cat’s interactions with mice by locating the Because we have a word for it, many people believe interactions on a linear scale, with total aggressiveness at that “intelligence” is a real entity. Yet, it is a complex one end, total defensiveness at the other, and various pro- construct that was developed by psychologists. Treating portions of the two in between. a psychological construct (e.g., intelligence) as if it Pellis and colleagues tested their conclusions by reduc- actually exists is a logical error, known as an error of ing the defensiveness of the cats with an antianxiety drug. reification. Have you ever encountered such errors in the popular media? Give an example. As predicted, the drug moved each cat along the scale toward more efficient killing. Cats that avoided mice before the injection “played with” them after the injection, those that “played with” them before the injection killed them Types of Aggressive and Defensive after the injection, and those that killed them before the Behaviors injection killed them more quickly after the injection. Based on the numerous detailed descriptions of LO 17.4 Describe the work that led to the distinction aggressive and defensive behaviors provided by the between aggressive and defensive behaviors Blanchards, Pellis and colleagues, and other biopsycholo- in mammals. gists who have followed their example, most research- Considerable progress in the understanding of aggres- ers now distinguish among different categories of such sive and defensive behaviors has come from the research ­behaviors. These categories of aggressive and defensive of Blanchard and Blanchard (see Blanchard, Summers, behaviors are based on three criteria: (1) their topography & Blanchard, 2013; Koolhaas et al., 2013) on the colony (form), (2) the situations that elicit them, and (3) their intruder model of aggression and defense in rats. Blanchard and apparent function. Several of these categories for rats are Blanchard have derived rich descriptions of rat intraspecific described in Table 17.2 (see Blanchard et al., 2011; Jager aggressive and defensive behaviors by studying the interac- et al., 2017; Kim & Jung, 2018). tions between the alpha male—the dominant male—of an The analysis of aggressive and defensive behaviors has established mixed sex colony and a small male intruder: led to the development of the target-site concept—the idea Upon encountering the intruder, the alpha male typically that the aggressive and defensive behaviors of an animal chases it away, repeatedly biting its back during the pursuit. are often designed to attack specific sites on the body of The intruder eventually stops running and turns to face the another animal while protecting specific sites on its own. alpha male. The intruder then rears up on its hind legs, still For example, the behavior of a socially aggressive rat (e.g., facing its attacker and using its forelimbs to ward off the lateral attack) appears to be designed to deliver bites to the attack. In response, the alpha male changes to a lateral ori- defending rat’s back and to protect its own face, the likely entation, with the side of its body perpendicular to the front target of a defensive attack. Conversely, most of the maneu- of the defending intruder. Then, the alpha moves sideways vers of the defending rat (e.g., boxing and pivoting) appear toward the intruder, crowding and trying to push it off bal- to be designed to protect the target site on its back. ance. If the defending intruder stands firm against this “lat- The discovery that aggressive and defensive behaviors eral attack,” the alpha often reacts by making a quick lunge occur in a variety of stereotypical species-common forms around the defender’s body in an attempt to bite its back. was the necessary first step in the identification of their neu- In response to such attacks, the defender pivots on its hind ral bases. Because the different categories of aggressive and feet, in the same direction as the attacker is moving, con- defensive behaviors are mediated by different neural cir- tinuing its frontal orientation to the attacker in an attempt cuits, little progress was made in identifying these circuits to prevent the back bite. before the categories were first delineated. For example, Another excellent illustration of how careful obser- the lateral septum was once believed to inhibit all aggres- vation of behavior has led to improved understanding of sion, because lateral septal lesions rendered laboratory rats aggressive and defensive behaviors is provided by Pellis notoriously difficult to handle—the behavior of the lesioned and colleagues’ (1988) study of cats. They began by video- rats was commonly referred to as septal aggression or septal taping interactions between cats and mice. They found that rage. However, we now know that lateral septal lesions do different cats reacted to mice in different ways: Some were not increase aggression: Rats with lateral septal lesions do efficient mouse killers, some reacted defensively, and some not initiate more attacks, but they are hyperdefensive when seemed to play with the mice. Careful analysis of the “play” threatened. M17_PINE1933_11_GE_C17.indd 470 22/01/2021 11:48  Biopsychology of Emotion, Stress, and Health 471 Table 17.2 Categories of Aggressive and Defensive Behaviors in Rats Aggressive Predatory Aggression The stalking and killing of members of other species for the purpose of eating them. Rats Behaviors kill prey, such as mice and frogs, by delivering bites to the back of the neck. Social Aggression Unprovoked aggressive behavior that is directed at a conspecific (member of the same species) for the purpose of establishing, altering, or maintaining a social hierarchy. In mammals, social aggression occurs primarily among males. In rats, it is characterized by piloerection, lateral attack, and bites directed at the defender’s back. Defensive Intraspecific Defense Defense against social aggression. In rats, it is characterized by freezing and flight and by Behaviors various behaviors, such as boxing, that are specifically designed to protect the back from bites. Defensive Attacks Attacks that are launched by animals when they are cornered by threatening members of their own or other species. In rats, they include lunging, shrieking, and biting attacks that are usually directed at the face of the attacker. Freezing and Flight Responses that many animals use to avoid attack. For example, if a human approaches a wild rat, it will often freeze until the human penetrates its safety zone, whereupon it will explode into flight. Maternal Defensive Behaviors The behaviors by which mothers protect their young. Despite their defensive function, they are similar to male social aggression in appearance. Risk Assessment Behaviors that are performed by animals in order to obtain specific information that helps them defend themselves more effectively. For example, rats that have been chased by a cat into their burrow do not emerge until they have spent considerable time at the entrance scanning the surrounding environment. Defensive Burying Rats and other rodents spray sand and dirt ahead with their forepaws to bury dangerous objects in their environment, to drive off predators, and to construct barriers in burrows. Aggression and Testosterone In some species, castration has no effect on social aggres- sion; in still others, castration reduces social aggression LO 17.5 Describe the relation between testosterone during the breeding season but not at other times. levels and aggression in males. The relation between aggression and testosterone lev- The fact that social aggression in many species occurs more els is difficult to interpret because engaging in aggres- commonly among males than among females is usually sive activity can itself increase testosterone levels—for explained with reference to the organizational and acti- example, just playing with a gun increased the tes- vational effects of testosterone (see Chapter 13). The brief tosterone levels of male college students (Klinesmith, period of testosterone release that occurs around birth in Kasser, & McAndrew, 2006). genetic males is thought to organize their nervous systems The blood level of testosterone, which is the only mea- along masculine lines and hence to create the potential for sure used in many studies, is not the best measure. male patterns of social aggression to be activated by the What matters more are the testosterone levels in the rel- high testosterone levels that are present after puberty. These evant areas of the brain. Although studies focusing on organizational and activational effects have been demon- brain levels of testosterone are rare, it has been shown strated in some mammalian species. For example, neonatal that testosterone can be synthesized in particular brain castration of male mice eliminates the ability of testoster- sites and not in others. one injections to induce social aggression in adulthood, and adult castration eliminates social aggression in male It is unlikely that humans are an exception to the usual mice that do not receive testosterone replacement injections. involvement of testosterone in mammalian social aggres- Unfortunately, research on testosterone and aggression in sion. However, the evidence is far from clear. In human other species has not been so straightforward (see Carré & males, aggressive behavior does not increase at puberty as Olmstead, 2015). testosterone levels in the blood increase; aggressive behav- The extensive comparative research literature on tes- ior is not eliminated by castration; and it is not increased by tosterone and aggression has been reviewed several times testosterone injections that elevate blood levels of testoster- (Demas et al., 2005; Munley, Rendon, & Demas, 2018; Soma, one. A few studies have found that violent male criminals 2006). Here are the major conclusions: (see Fragkaki, Cima, & Granic, 2018) and aggressive male and female athletes tend to have higher testosterone levels Testosterone increases social aggression in the males of than normal (see Batrinos, 2012; Denson et al., 2018); how- many species; aggression is largely abolished by castra- ever, this correlation may indicate that aggressive behaviors tion in these same species (see Hashikawa et al., 2018). increase testosterone, rather than vice versa. M17_PINE1933_11_GE_C17.indd 471 22/01/2021 11:48  472 Chapter 17 The lack of strong evidence of the involvement of tes- a tone, but bilateral lesions to the auditory cortex did not. tosterone in human aggression could mean that hormonal This indicated that for auditory fear conditioning to occur, and neural regulation of aggression in humans differs from it is necessary for signals elicited by the tone to reach the that in many other mammalian species. Or, it could mean medial geniculate nucleus but not the auditory cortex. It that the research on human aggression and testosterone is also indicated that a pathway from the medial geniculate flawed. For example, human studies are typically based on nucleus to a structure other than the auditory cortex plays a blood levels of testosterone (often inferred from saliva levels key role in fear conditioning. This pathway proved to be the because collecting saliva is safer and easier than collecting pathway from the medial geniculate nucleus to the amyg- blood) rather than on brain levels. However, the blood lev- dala. Lesions of the amygdala, like lesions of the medial els of a hormone aren’t necessarily indicative of how much geniculate nucleus, blocked auditory fear conditioning. The hormone is reaching the brain. Also, the researchers who amygdala receives input from all sensory systems, and it is study human aggression have often failed to appreciate the believed to be the structure in which the emotional signifi- difference between social aggression, which is related to tes- cance of sensory signals is learned and retained. tosterone in many species, and defensive attack, which is Several pathways carry signals from the amygdala to not (see Montoya et al., 2012; Sobolewski, Brown, & Mitani, brain stem structures that control the various emotional 2013). Most seemingly aggressive outbursts in humans are responses (see Dampney, 2015). For example, a pathway to overreactions to real or perceived threat, and thus they are the periaqueductal gray of the midbrain elicits appropriate more appropriately viewed as defensive attack, not social defensive responses (see Kim et al., 2013), whereas another aggression. pathway to the lateral hypothalamus elicits appropriate sympathetic responses. The fact that auditory cortex lesions do not disrupt fear conditioning to simple tones does not mean that the Neural Mechanisms of Fear auditory cortex is not involved in auditory fear condition- ing. There are two pathways from the medial geniculate Conditioning nucleus to the amygdala: the direct one, which you have Much of what we know about the neural mechanisms of already learned about, and an indirect one that projects via fear has come from the study of fear conditioning. Fear the auditory cortex. Both routes are capable of mediating conditioning is the establishment of fear in response to a fear conditioning to simple sounds; if only one is destroyed, previously neutral stimulus (the conditional stimulus) by pre- conditioning progresses normally. However, only the corti- senting it, usually several times, before the delivery of an cal route is capable of mediating fear conditioning to com- aversive stimulus (the unconditional stimulus). plex sounds (see Chang & Grace, 2015). In a standard fear conditioning experiment, the sub- Figure 17.9 illustrates the circuit of the brain that is ject, often a rat, hears a tone (conditional stimulus) and then thought to mediate the effects of fear conditioning to an receives a mild electric shock to its feet (unconditional stim- auditory conditional stimulus (see Calhoun & Tye, 2015; ulus). After several pairings of the tone and the shock, the Herry & Johansen, 2014). The sound signal from an audi- rat responds to the tone with a variety of defensive behav- tory conditional stimulus travels from the medial geniculate iors (e.g., freezing and increased susceptibility to startle) nucleus of the thalamus to reach the amygdala directly, or and sympathetic nervous system responses (e.g., increased indirectly via the auditory cortex. The amygdala assesses heart rate and blood pressure). LeDoux and his colleagues the emotional significance of the sound on the basis of pre- have mapped the neural mechanism that mediates this vious encounters with it, and then the amygdala activates form of auditory fear conditioning (see Kim & Jung, 2018; the appropriate response circuits—for example, behavioral Ledoux, 2014). circuits in the periaqueductal gray and sympathetic circuits in the hypothalamus. Amygdala and Fear Conditioning Contextual Fear Conditioning and LO 17.6 Describe the role of the amygdala in fear conditioning. the Hippocampus LO 17.7 Describe the role of the hippocampus in LeDoux and his colleagues began their search for the neu- contextual fear conditioning. ral mechanisms of auditory fear conditioning (fear condition- ing that uses a sound as a conditional stimulus) by making Environments, or contexts, in which fear-inducing stimuli lesions in the auditory pathways of rats. They found that are encountered can come to elicit fear. For example, if you bilateral lesions to the medial geniculate nucleus (the auditory repeatedly encountered a bear on a particular trail in the relay nucleus of the thalamus) blocked fear conditioning to forest, the trail itself would begin to elicit fear. The process M17_PINE1933_11_GE_C17.indd 472 22/01/2021 11:48  Biopsychology of Emotion, Stress, and Health 473 conditional stimulus. For example, if a rat receives shocks Figure 17.9 The structures thought to mediate the sym- pathetic and behavioral responses conditioned to an auditory in a distinctive test chamber, the rat will become fearful of conditional stimulus. that chamber. In view of the fact that the hippocampus plays a key role in memory for spatial location, it is reasonable to expect that it would be involved in contextual fear conditioning. This seems to be the case (see Chaaya, Battle, & Johnson, Thalamus 2018; Maren, Phan, & Liberzon, 2013). Bilateral hippocam- pal lesions block the subsequent development of a fear Medial geniculate response to the context without blocking the development nucleus of a fear response to the explicit conditional stimulus (e.g., Auditory cortex a tone; see Moscarello & Maren, 2018). Hypothalamus Amygdala Amygdala Complex and Fear Conditioning THREATENING PAG LO 17.8 Describe the role of two specific amygdalar SOUND nuclei in fear conditioning. The preceding discussion has probably left you with the impression that the amygdala is a single brain structure; it SYMPATHETIC BEHAVIORAL isn’t. It is actually a cluster of many nuclei, often referred RESPONSE RESPONSE to as the amygdala complex. The amygdala is composed of a dozen or so major nuclei, which are themselves divided into subnuclei. Each of these subnuclei is structurally dis- tinct, has different connections, and is thus likely to have by which benign contexts come to elicit fear through their different functions (see Duvarci & Pare, 2014; Janak & association with fear-inducing stimuli is called contextual Tye, 2015). fear conditioning. The study of fear conditioning provides a compelling demonstration of the inadvisability of assuming that the amygdala is a single structure. Evidence has been accumu- Journal Prompt 17.2 lating that the lateral nucleus of the amygdala—not the Can you think of an instance where you have been entire amygdala—is critically involved in the acquisition, ­subjected to contextual fear conditioning? Describe that instance. storage, and expression of conditioned fear (see Duvarci & Pare, 2014; Janak & Tye, 2015; Tovote, Fadok, & Lüthi, 2015). Both the prefrontal cortex and the hippocampus project to Contextual fear conditioning has been produced in the lateral nucleus of the amygdala: The prefrontal cortex the laboratory in two ways. First, it has been produced by is thought to act on the lateral nucleus of the amygdala to the conventional fear conditioning procedure, which we suppress conditioned fear (see Gilmartin, Balderston, & just discussed. For example, if a rat repeatedly receives an ­Helmstetter, 2014), and the hippocampus is thought to inter- electric shock following a conditional stimulus, such as a act with that part of the amygdala to mediate learning about tone, the rat will become fearful of the conditional context the context of fear-related events. The amygdala is thought (the test chamber) as well as the tone. Second, contextual to control defensive behavior via outputs from the central fear conditioning has been produced by delivering aversive nucleus of the amygdala (see Janak & Tye, 2015; Kim & stimuli in a particular context in the absence of any other Jung, 2018; Pellman & Kim, 2016; Ressler & Maren, 2019). Scan Your Brain This chapter is about to change direction: The remaining two introductory material on emotion and fear. Fill in each of the modules focus on the neural mechanisms of human emotion following blanks with the most appropriate term. The correct and on the effects of stress on health. This is a good point answers are provided at the end of the exercise. Before con- for you to scan your brain to see whether it has retained the tinuing, review material related to your errors and omissions. M17_PINE1933_11_GE_C17.indd 473 22/01/2021 11:48  474 Chapter 17 1. Bard discovered that the _______ is critical for the 8. Two muscle groups, orbicularis oculi and _______, have expression of aggressive responses. been identified to depict a Duchenne smile. 2. Emotional processing is supported by a circuit in the 9. The emotional reaction to threat is _______. brain called the _______. 10. _______ increases aggression in the males of many 3. In primates, most of the symptoms of Klüver–Bucy ­species, and castration decreases it. ­syndrome are the result of damage to the _______. 11. In a standard _______ task, a previously neutral stimulus 4. _______ theory suggests that an emotional event triggers is paired with an aversive stimulus. autonomic activity and behavior, which then produce the 12. The _______ plays a key role in memory for spatial feeling of emotion. locations. 5. _______ is a method of interrogation that uses changes 13. Projections from the _______ _______ to the amygdala to the ANS to detect lies in a person’s responses. act to suppress conditioned fear. 6. There are six primary emotions: happiness, anger, fear, (11) fear-conditioning, (12) hippocampus, (13) prefrontal cortex. surprise, sadness, and _______. ­feedback, (8) zygomaticus major, (9) fear, (10) Testosterone, 7. According to the _______ _______ hypothesis, facial (3) amygdala, (4) James-Lange, (5) Polygraph, (6) disgust, (7) facial expressions may alter our emotional state. Scan Your Brain answers: (1) hypothalamus, (2) limbic system, ­ iffuse—there is not a c­ enter for each emotion (see d Brain Mechanisms of ­F einstein, 2013). Think “mosaic,” not “­ center,” for ­locations of brain mechanisms of emotion. Human Emotion There is virtually always activity in motor and sensory cortices when a person experiences an emotion. This module deals with the brain mechanisms of human Similar patterns of brain activity tend to be recorded emotion. We still do not know how the human brain controls when a person experiences an emotion, imagines the experience or expression of emotion, or how the brain that emotion, or sees somebody else experience that interprets emotion in others, but progress has been made. ­emotion (see Figure 17.10). Each of the following sections illustrates an area of progress. Figure 17.10 Horizontal, sagittal, and coronal functional MRIs show areas of Cognitive increased activity in the primary motor cortex (M1) and the premotor cortex (PMC) Neuroscience when volunteers watched facial expressions of emotion. The same areas were active when the volunteers made the expressions themselves. of Emotion LO 17.9 Describe the current status of cognitive neuroscience research on emotion. Cognitive neuroscience is currently the dominant approach being used to study the brain mechanisms of human emotion. There have been many functional brain imaging stud- ies of people experiencing or imag- ining emotions or watching others experiencing them. These studies have established three points that have advanced our understanding of the brain mechanisms of emotion in fundamental ways (see Neumann et al., 2014; Wood et al., 2016): Brain activity associated From Carr et al., 2003, Neural Mechanisms of Empathy, 100, pgs. 5497-5502. Figure 1 on page 550. Copyright with each human emotion is (2003) National Academy of Sciences, U.S.A. M17_PINE1933_11_GE_C17.indd 474 22/01/2021 11:48  Biopsychology of Emotion, Stress, and Health 475 These three fundamental findings are influencing or extracting information from them (e.g., information about age how researchers are thinking about the neural mecha- or gender). However, S.P. did have a severe postsurgical deficit nisms of emotion. For example, the activity observed in in recognizing facial expressions of fear and less striking defi- sensory and motor cortex during the experience of human cits in recognizing facial expressions of disgust, sadness, and happiness. emotions is now believed to be an important part of the In contrast, S.P. had no difficulty specifying which emotion mechanism by which the emotions are experienced. The would go with particular sentences. Also, she had no difficulty re-experiencing of related patterns of motor, autonomic, using facial expressions upon request to express various emo- and sensory neural activity during emotional experiences tions (see Anderson & Phelps, 2000). is generally referred to as the embodiment of emotions (see Wang et al., 2016). The case of S.P. is similar to reported cases of Urbach- Amygdala and Human Emotion Wiethe disease (see Meletti et al., 2014). Urbach-Wiethe LO 17.10 Describe the role of the amygdala in human ­disease is a genetic disorder that often results in c­ alcification emotion. (hardening by conversion to calcium carbonate, the main component of bone) of the amygdala and surrounding ante- You have already learned that the amygdalae play an rior medial temporal lobe structures in both hemispheres. important role in fear conditioning in rats. Numerous One Urbach-Wiethe patient with bilateral amygdalar ­functional brain-imaging studies have suggested that damage was found to have lost the ability to recognize facial the function of the human amygdalae is more general. expressions of fear (see Adolphs, 2006). Indeed, she could not Although the human amygdalae appear to respond most describe fear-inducing situations or produce fearful expres- robustly to fear, they also respond to other emotions (see sions, although she had no difficulty on tests involving other Hsu et al., 2015; Koelsch & Skouras, 2014; Patin & Pause, emotions. 2015). Indeed, the amygdalae appear to play a role in the performance of any task with an emotional component, whether positive or negative (see Fastenrath et al., 2014; Medial Prefrontal Lobes and Human Stillman, Van Bavel, & Cunningham, 2015). This has led to the view that the amygdalae play a role in evaluating the Emotion emotional significance of situations. LO 17.11 Describe the role of the medial prefrontal Although the results of brain-imaging studies sug- lobes in human emotion. gest that the amygdalae play a general role in emotions, Emotion and cognition are often studied independently, the study of some patients with amygdalar damage sug- but it is now believed that they are better studied as differ- gests a specific role in fear. The following case illustrates ent components of the same system (see Barrett & Satpute, this point. 2013). The medial portions of the prefrontal lobes (including the medial portions of the orbitofrontal cortex and anterior cingulate cortex) are the sites of emotion–­cognition inter- The Case of S.P., the Woman action that have received the most attention (e.g., Etkin, Who Couldn’t Perceive Fear Büchel, & Gross, 2015; Hiser & Koenigs, 2017; Kragel et al., 2018). Functional brain-imaging studies have found At the age of 48, S.P. had her right amygdala and adjacent evidence of activity in the medial prefrontal lobes when tissues removed for the treatment of epilepsy. Because her emotional reactions are being cognitively suppressed or left amygdala had been damaged, she in effect had a bilateral re-evaluated (see Okon-Singer et al., 2015). amygdalar lesion. Many studies of medial prefrontal lobe activity employ suppression paradigms or reappraisal paradigms. Journal Prompt 17.3 In studies that use suppression paradigms, participants Before reading any further, based on the animal are directed to inhibit their emotional reactions to unpleas- research on the amygdala that you read about in ant films or pictures; in studies that use reappraisal the previous module, try to predict the sorts of ­paradigms, participants are instructed to reinterpret a pic- ­deficits you would expect to see in patient S.P. ture to change their emotional reaction to it. The medial prefrontal lobes are active when both of these paradigms Following her surgery, S.P. had an above average I.Q., and are used, and they seem to exert their cognitive control of her perceptual abilities were generally normal. Of particular rel- emotion by interacting with the amygdala (see Whalen evance was the fact that she had no difficulty in identifying faces et al., 2013). M17_PINE1933_11_GE_C17.indd 475 22/01/2021 11:48  476 Chapter 17 Many theories of the specific functions of the medial lateralization of emotion have employed functional prefrontal lobes have been proposed. The medial prefron- brain-imaging methods, and the results have been com- tal lobes have been hypothesized to monitor the difference plex and variable. Wager and colleagues (2003) per- between outcome and expectancy (see Diekhof et al., 2012), formed a meta analysis of the data from 65 such studies. to encode stimulus value over time (Tsetsos et al., 2014), to The main conclusion of Wager and colleagues was predict the likelihood of error (see Hoffmann & Beste, 2015), that the current theories of lateralization of emotion are too to mediate the conscious awareness of emotional stimuli general from a neuroanatomical perspective. Overall com- (see Mitchell & Greening, 2011), and to mediate social parisons between left and right hemispheres revealed no decision making (see Lee & Seo, 2016; Phelps, Lempert, & interhemispheric differences in either the amount of emo- ­Sokol-Hessner, 2014). Which hypothesis is correct? Perhaps tional processing or the valence of the emotions being pro- all are; the medial prefrontal cortex is large and complex, cessed. However, when the comparisons were conducted and it likely performs many functions. This point was made on a structure-by-structure basis, they revealed substantial by the study of Kawasaki and colleagues (2005). evidence of lateralization of emotional processing. Some Kawasaki and colleagues used microelectrodes to kinds of emotional processing were lateralized to the left record from 267 neurons in the anterior cingulate cortices hemisphere in certain structures and to the right in others. (part of the medial prefrontal cortex) of four patients prior ­Functional brain-imaging studies of emotion have commonly to surgery. They assessed the activity of the neurons when observed lateralization in the amygdalae—more activity is the patients viewed photographs with emotional content. often observed in the left amygdala. Clearly, n ­ either the right Of these 267 neurons, 56 responded most strongly and hemisphere model nor the valence model of the lateraliza- consistently to negative emotional content. This confirms tion of emotion is supported by the evidence. The models previous research linking the medial prefrontal lobes with are too general. negative emotional reactions, but it also shows that not all Another approach to studying the lateralization neurons in the area perform the same function—neurons of emotions is based on observing the asymmetry of directly involved in emotional processing appear to be facial expressions. In most people, each facial expres- sparse and widely distributed in the human medial pre- sion begins on the left side of the face and, when fully frontal lobes. expressed, is more pronounced there—which implies