The Hazards of Fearlessness "Fear has its use, but cowardice has none," wrote the Mahatma Gandhi. But wouldn't it be great to never feel fear at all? When we say that heroes are "fearless," what we really mean is that they manage to function effectively despite the fear they experience, not that they never feel afraid. However, there are people who literally do not experience fear. One such woman, known as S.M. in the scientific literature, lost her ability to feel fear in late childhood because of a genetic disorder so rare, fewer than 300 cases have been reported (Feinstein et al., 2011). In Chapter 5 we saw how the absence of an unpleasant experience, pain, can be hazardous to your health. S.M. similarly shows us the survival value of fear. Not only is she unafraid of snakes or spiders, but she once walked right up to a knife-wielding robber and basically dared him to stab her. He was so disquieted by her strange response that he ran away! Another time she was nearly killed in an act of domestic violence. While her behavioral responses and self-report appear typical for other emotions, S.M. shows very little of the physiological response, organized by the sympathetic nervous system,
that the rest of us experience in response to frightening situations. Similarly, S.M. produces almost no startle response to a sudden, loud noise (Aschwanden, 2013), and she seems not to notice expressions of fear in the faces of other people (L. F. Barrett, 2018). S.M. is not deliberately reckless; she has learned to follow simple safety rules like looking both ways before crossing the street. But there are other consequences of S.M.'s fearlessness that you might not predict. When talking to someone, she tends to get much closer than other people do, sometimes just a foot away (D. P. Kennedy et al., 2009). When strangers talk to her in public, like the mugger she encountered, she tends to stroll right up to them. S.M. also fails to perceive risk in more mundane social situations, so she's an easy target for internet scams. Although she's very outgoing and might fondly address a waiter she's only met once before, she has few long-term friendships, perhaps because she speaks without caution. Maybe being fearless isn't all it's cracked up to be. What happened to S.M. to make her this way, and is there really nothing she is afraid of?
Our chapter begins with a discussion of physiological and behavioral processes involved in varying emotional states, and then we turn to a more in-depth look at fear and aggression because both are important for survival and they are readily studied in animals. We'll then end the chapter by turning to one of the products of aggression--stress--and the impacts of stress on neural function.
emotion A subjective mental state that is usually accompanied by distinctive cognition, behaviors, and physiological changes. sympathetic nervous system The part of the autonomic nervous system that acts as the fight-or-flight system, generally preparing the body for action. parasympathetic nervous system The part of the autonomic nervous system that generally prepares the body to relax and recuperate. View Animation 11.2: Brain Explorer Fear and Loathing Can Save You Strong emotions, like fear in unfamiliar and threatening circumstances, are evolved adaptations that swiftly activate behavioral and physiological responses appropriate to the situation.
11.1Theories of Emotion Integrate Physiological and Behavioral Processes We start by looking at theoretical accounts of the perception of emotions, and the display of emotion via facial expressions. After reading this section, you should be able to: 11.1.1 Describe and compare the dominant theories of the relationship between emotion and physiological changes. 11.1.2 Discuss the integration of autonomic responses with the perception of specific emotions. 11.1.3 Review the evidence for a core set of emotions as well as their role in guiding preprogrammed responses to environmental challenges. 11.1.4 Discuss the role of facial expressions of emotion, the ways in which cultural differences influence facial displays, and the neural pathways that control facial expressions. 11.1.5 Discuss the pros and cons of trying to measure emotional states using techniques like polygraphy. Ranging from soaring joy to the depths of fear and loathing, our emotions are evolved programs that guide our responses to daily threats and opportunities. The topic of emotions is complicated by the fact that we apply the word emotion to several different things. Emotion is a private, subjective feeling that we may have without anyone else being aware of it. But the word emotional is also used to describe many behaviors that people show, such as fearful facial expressions, frantic arm movements, or angry shouting. Emotion may influence, and be influenced by, cognitive processes like memory and attention. Furthermore, during strong emotion we often experience physiological changes, such as a rapidly beating heart, shortness of breath, or excessive sweating. To encompass all four aspects of emotion, we will define emotion as a subjective mental state that is usually accompanied by distinctive cognition, behaviors, and physiological changes. In many emotional states the heart races, the hands and face become warm, the palms sweat, and the stomach feels queasy. Common expressions capture this emotional-physical association: "my hair stood on end," "a sinking feeling in my stomach." These sensations are the result of activation of the autonomic nervous system--either the sympathetic nervous system (the "fight-or-flight" system that generally activates the body for action) or the parasympathetic nervous system (which generally prepares the body to relax and recuperate) (see Figure 1.9). Several theories have tried to explain the close ties between the subjective feelings of emotions and the activity of the autonomic nervous system. Common sense suggests that the autonomic reactions are caused by the emotion--"I was so angry, my hands were shaking"--as though the anger produces the shaking (FIGURE 11.1A). Yet research indicates that the relationship between emotion and physiological arousal is more subtle. Do emotions cause bodily changes, or vice versa? William James (1842-1910) and Carl Lange (1834-1900) turned the commonsense notion on its head, suggesting that the emotions we experience are caused by the bodily changes. From this perspective, we experience fear because we perceive the activity that dangerous conditions trigger in our body (FIGURE 11.1B). Different emotions thus feel different because they are generated by different constellations of physiological responses. The James-Lange theory inspired many attempts to link specific emotions to specific bodily responses. These attempts mostly failed because it turns out that there is
Emotions, Aggression, and Stress 351 no distinctive autonomic pattern for each emotion. Fear, surprise, and anger, for example, tend to be accompanied by sympathetic activation, while parasympathetic activation tends to accompany both joy and sadness. In addition, the physiological reactions are rather slow, as physiologists Walter Cannon (1871-1945) and Philip Bard (1898-1977) pointed out (W. B. Cannon, 1929). According to the Cannon-Bard theory, it is the brain's job to decide which particular emotion is an appropriate response to the stimuli. According to this model, the cerebral cortex simultaneously decides on the appropriate emotional experience (fear, surprise, joy) and activates the autonomic nervous system to appropriately prepare the body, using either the parasympathetic system to help the body relax, or the sympathetic system to ready the body for action (FIGURE 11.1C).
(A) Folk psychology (feeling triggers autonomic reaction)
Informal observation suggested that emotions cause the body to react.
(B) James-Lange theory (autonomic reaction triggers feeling)
James and Lange argued that the bodily response evokes the emotional experience.
Speci c pattern of autonomic arousal (heart races, etc.)
Speci c pattern of autonomic arousal (heart races, etc.) Particular emotion experienced (fear)
(C) Cannon-Bard theory (simultaneous feeling and autonomic reaction)
Cannon and Bard insisted that the brain must interpret the situation to decide which emotion is appropriate.
General autonomic arousal (heart races, etc.) Particular emotion experienced (fear)
Bodily response and emotional experience are simultaneous.
(D) Schachter & Singer theory (cognitive attribution of emotion to arousal)
Schachter and Singer propose that we use context to cognitively attribute speci c emotions to arousal.
Speci c pattern of autonomic arousal (heart races, etc.)
FIGURE 11.1 Different Views of the Chain of Events in Emotional Responses
Attribution of emotion responsible for arousal
Do we use context to attribute specific emotions to physiological arousal?
Like Cannon and Bard, Stanley Schachter and Jerome Singer (Schachter and Singer, 1962; Schachter, 1975) emphasized cognitive mechanisms in emotion. Under this model, however, emotional labels (e.g., anger, fear, joy) are attributed to relatively nonspecific feelings of physiological arousal (FIGURE 11.1D). The specific emotion we experience is thought to depend on cognitive systems that assess the context--our current social, physical, and psychological situation. In a famous test of this idea, participants were injected with epinephrine (adrenaline) and told either that there would be no effect or that their hearts would race (Schachter and Singer, 1962). Participants who were warned of this physiological reaction reported no emotional experience--presumably because they
attributed the arousal to the injection rather than to an emotion-- but some participants who were not forewarned experienced emotions when their bodies responded to the drug. Presumably, the participants who weren't forewarned misattributed their racing hearts to their current emotional context, rather than to the injection. However, exactly which emotion was experienced could be affected by whether another person in the room (secretly an actor) acted angry or happy. The unsuspecting participants injected with epinephrine were much more likely to report feeling angry when in the presence of an "angry" confederate, and more likely to report feeling elated when paired with a "happy" confederate (FIGURE 11.2A).
FIGURE 11.2 The Classic Schachter and Singer Experiment
Hypothesis Circumstances provoke autonomic arousal; we then attribute arousal to a particular emotion on the basis of context. Test Activate the sympathetic nervous system with an injection of epinephrine to see whether the participants, uninformed about the drug's effects, experience one particular emotion as they fill out some forms. To test the hypothesis that our emotional experience is determined by cognitive processes, expose the participants to a confederate who acts either angry or happy while filling out the forms. (A)
Playful confederate Some participants are exposed to a playful confederate while filling out the form.
Other participants are exposed to an angry confederate while filling out the form.
These participants were more likely to report feeling elated.
These participants were more likely to report feeling angry and frustrated.
Result Participants who were warned that the injection might affect heart rate reported no emotional reaction. Participants who were not warned about the sympathetic arousal reported more intense emotional reactions than those who were given a control injection. However, among the participants who were not warned about the effects of the injection, which emotion they experienced (angry or happy) tended to match that of the confederate.
Conclusion While autonomic responses can intensify our emotional experience,
These participants were more likely to report feeling elated.
These participants were more likely to report feeling angry and frustrated.
Result Emotions, Aggression, and Stress 353 Participants who were warned that the injection might affect heart rate reported no emotional reaction. Participants who were not warned about the sympathetic arousal reported more intense emotional reactions than those who were given a control injection. However, among the participants who were not warned about the effects of the injection, which emotion they experienced (angry or happy) tended to match that of the confederate. RESEARCHERS AT WORK(continued)
Conclusion While autonomic responses can intensify our emotional experience, they cannot explain why we have different emotional experiences in different situations. Rather, our cognitive analysis of the environment affects which emotion we experience.
Emotion experienced will affect future interpretations of stimuli and continuing autonomic arousal.
General autonomic arousal (heart races, etc.) Autonomic responses contribute to the intensity of emotional experience. Particular emotion experienced (anger)
These findings contradict the James-Lange prediction that Watson/Breedlove The Mfeienldin'sgsMoafchainngeer or elation should each be associated with a Founudantiiqounseopf rBorfaiilen aonfdaBuethoanvoiomr 4ice reactions. Schachter and Singer concluded that the participants experienced their epinephrine-inMM4e_11.02 08/04/20 duced physiological arousal as whichever emotion seemed appropriate, based on their cognitive assessment of the situation: "My heart's really pounding; I'm so angry!" or "My heart's really pounding; I'm so elated!" depending on the environment. Thus, they said, our emotional states are the results of interaction between two factors: physiological arousal, and cognitive interpretation of the concurrent context, including social cues like other people's emotional expressions. (This emphasis on the combination of physiological arousal and cognitive interpretation is why Schachter and Singer's model is also known as the two-factor theory of emotion). The cognitive theory also suggests that our emotional experience at one time may affect how we interpret later events (FIGURE 11.2B).
Another interesting outcome of the Schachter and Singer experiment is that the participants receiving epinephrine reported experiencing more intense emotions than other participants who were given saline. This result conforms with the James-Lange view that autonomic responses intensify emotion but are nonspecific (G. W. Hohmann, 1966). More recent evidence, however, has explored whether patterns of autonomic activity systematically differ between broad classes of positive and negative emotions--for example, happiness versus fear versus sadness versus anger--suggesting that the Schachter and Singer model may not provide a complete explanation of the relationship between arousal and emotion (B. H. Friedman, 2010; E. H. Siegel et al., 2018). Nevertheless, it is because the sympathetic system is activated to some degree by any threatening situation that so-called lie detectors are very poor at distinguishing liars from truthful people who are anxious, as we discuss next in Signs & Symptoms.
SIGNS & SYMPTOMS Lie Detector? One of the most controversial attempts to apply biomedical science in legal settings is the so-called lie detector test. In this procedure, properly called a polygraph test (from the Greek poly, "many," and graphein, "to write"), multiple physiological measures are recorded in an attempt to detect lying during a carefully structured interview. The test is based on the assumption that people have emotional responses when lying because they fear detection and/or feel guilty about lying. Emotions are usually accompanied by bodily responses that are difficult to control, such as changes in respiratory rate, heart rate, blood pressure, and skin conductance (a measure of sweating). In
polygraph recordings like the one in FIGURE 11.3, each wiggly line, or trace, provides a measurement of one of these physiological variables. Taken together, the measurements are assumed to track the physiological arousal, over time, of the person being tested. When a person lies in response to a direct question (arrows), momentary changes in several of the measured variables may occur. People who administer polygraph examinations for a living claim that polygraphs are accurate in 85-95% of tests, but the estimate from impartial research is an overall accuracy of about 65% (Nietzel, 2000; Gougler et al., 2011). Even if the higher figure (Continued )
were correct, the fact that these tests are widely used would mean that thousands of truthful people could be branded as liars and fired, disciplined, or not hired. On the other hand, many criminals and spies have been able to pass the tests without detection (Wollan, 2015). For example, longtime CIA agent Aldrich Ames, who was sentenced in 1995 to life in prison for espionage, successfully passed polygraph tests after becoming a spy; former polygraph operators have even offered how-to guides to beating polygraph tests (www.polygraph.com). In the wake of the terrorist attacks of 2001, a federally appointed panel of scientists noted that even if polygraphs were correct 80% of the time (which is much higher than impartial research suggests), then giving the test to a group of 10,000 people that included 10 spies would condemn 1,600 innocent people-- and let 2 spies go free (National Academy of Sciences, 2003)! Some scientists believe that modern neuroscience may provide new methods of lie detection someday, perhaps using functional brain imaging technology such as PET or fMRI (Abe et al., 2007). However, attempts to use brain scanners as lie
detectors so far have yielded unreliable results (Rusconi and Mitchener-Nissen, 2013), and even if they are validated, such lie detectors will be more costly and less widely available than polygraphs.
FIGURE 11.3 The Polygraph Measures Signs of Arousal
Respiration Skin conductance Heart rate 10 20 30 40 50 60 70 80 90 100 110 120 Time (s)
polygraph Popularly but inaccurately referred to as a lie detector. A device that measures several bodily responses, such as heart rate and blood pressure.
Is there a core set of emotions? Just as the colors of the spectrum combine into subtle hues, researchers think there may be a core set of basic emotions underlying the more varied and delicate nuances of our world of feelings. In his book The Expression of the Emotions in Man and Animals (1872), Charles Darwin noted that certain expressions of emotions appear to be universal among people of all regions of the world. Furthermore, Darwin asked whether nonhuman animals may show comparable expressions of some emotions, arguing that aspects oWfaetsmono/tBioreneadlloevxepression may have originated in a common ancestor. The Mind's Machine He noted that noFnouhnudmatioanns opfrBirmaiantaensdhBaehvaevitohr 4eesame facial muscles that humans have, and a century later, Redican (1982) noted distinct facial expressions in nonhuman primates that appeaMreMd4teo_1s1ig.0n3al 0e5m/2o7t/io2n0 al states; for example, chimpanzees show a play face, which may be homologous to the human laugh (FIGURE 11.4). This connection may even extend beyond primates: for example, tickling and playing with rats can
© Nic van Oudtshoorn/Alamy Stock Photo © blickwinkel/Alamy Stock Photo
FIGURE 11.4 Facial Expression of Emotions in Nonhuman Primates
A juvenile chimpanzee shows a play face while being tickled. He also makes a guttural laughing sound.
The female chacma baboon on the left bares her teeth, grinning to signal submission to a dominant animal. In humans, teeth baring has gained a different, friendlier meaning.
Emotions, Aggression, and Stress 355 By processing many hours of video of mice in varying emotional circumstances, a computerized AI system learned to categorize the six subtle-but-distinct mouse facial expressions shown here. The facial expressions were associated with activity in brain mechanisms known to be involved in emotion in humans (Dolensek et al., 2020).
FIGURE 11.5 Facial Expressions in the Mouse (After N. Dolensek et al., 2020. Science 368: 89. Courtesy of Julia Kuhl.)
elicit ultrasonic vocalizations that resemble laughter, and playing may facilitate social
contact and learning (Panksepp, 2007; Burgdorf et al., 2008). Amazingly, even mice
make subtle but distinct emotion-related facial expressions, associated with activity in
neural mechanisms of emotion (FIGURE 11.5) (Dolensek et al., 2020).
So, why did emotions and their expression evolve, and how do they help individuals
survive and reproduce? Most of us have experienced the frightening nighttime percep-
tion of being stalked by a predator--real or imagined, human or nonhuman. Through
natural selection, a program for dealing with this situation evolved: we call that pro-
gram fear. The emotion of fear shifts our perception, attention, cognition, and action
to focus on avoiding danger and seeking safety, while preparing us physiologically
for fighting or fleeing. Other activities, such as seeking food, sleep, or mates, are sup-
pressed. In the face of an imminent threat to survival, it is better to be afraid, thereby
activating a recipe for action that was developed and
tested over the ages, than to ad-lib something new. Viewed in this way, emotions can be seen as
evolved preprogramming that helps us deal quickly and effectively with a wide variety of situations. As another example, feelings of disgust for body fluids may
help us avoid exposure to germs (Curtis et al., 2004),
so it may be wise to recognize disgust in others. Our
human tendency to make snap judgments about other
people, based on their appearance and facial expres-
sions, may be an unfortunate overgeneralization of mechanisms that evolved to help us recognize signs of
Watstohnr/eBarteoedr ldoavenger from others (Todorov et al., 2008).
The MindO'snMeafcohrinmeulation (Plutchik, 2001) proposes there Foundations of Brain and Behavior 4e are eight basic emotions, grouped in four pairs of opMMp4eo_s1i1t.e05s--0jo6/y1/7s/a2d0ness, affection/disgust, anger/fear,
and expectation/surprise--with all other emotions arising from combinations of this basic array (FIGURE 11.6). But researchers do not yet agree about the num-
ber of basic emotions (six, seven, eight?). While there may be no way to determine once and for all the number of basic emotions, one clue comes from examining the number of different kinds of facial expressions
that we produce and can recognize in others.
According to one popular scheme, the eight basic emotions are arrayed as four pairs of opposite emotions. Lower- and higherintensity forms of each basic emotion appear at the bottom and top levels, respectively.
Facial expressions have complex functions in communication How many different emotions can be detected in facial expressions? According to Paul Ekman and collaborators, there are distinctive expressions for anger, sadness, happiness, fear, disgust, surprise, contempt,
FIGURE 11.6 One Classification of Basic Emotions (After R. Plutchik, 1994. The psychology and biology of emotion. HarperCollins. New York, NY.)
According to Paul Ekman and colleagues, the basic emotional facial expressions shown here are displayed in all cultures.
FIGURE 11.7 The Eight Universal Facial Expressions of Emotion
and embarrassment (FIGURE 11.7) (Keltner and Ekman, 2000). Facial expressions of these emotions are interpreted similarly across many cultures without explicit training. (In case you're keeping track, whereas Plutchik included affection and expectation in his eight basic emotions, Keltner and Ekman include, instead, facial expressions of contempt and embarrassment. The other six emotions--anger, sadness, happiness, fear, disgust, and surprise--are recognized in both schemes.)
People from Western and non-Western literate
represented by photographs of facial expressions.
But people from isolated nonliterate groups are less likely to agree with those judgments about some facial expressions, especially of surprise and disgust.
The white bars indicate the percentage of agreement that would be expected by chance alone.
0 Ha Su An Sa Fe Di Western literate (20 groups)
Ha Su An Sa Fe Di Non-Western literate (11 groups)
Ha Su An Sa Fe Di Isolated nonliterate (3 groups)
FIGURE 11.8 Cultural Differences in Recognizing Facial Expressions of Emotion (After J. A. Russell, 1994. Psychol. Bull. 115: 102.)
Elicitors Actual or anticipated situations, recollections, etc.
Facial affect program (pan-cultural) Facial motor programs for: Happiness Surprise Anger Sadness Fear Disgust Embarrassment Contempt
Mediation by culture-speci c display rules Exaggerate Minimize Counteract Camou age
Emotions, Aggression, and Stress 357 End result
FIGURE 11.9 A Model for Emotional Facial Expressions across Cultures
Cross-cultural similarity is also noted in the production of expressions specific to particular emotions. For example, people in a nonliterate New Guinea society show emotional facial expressions like those of people in industrialized societies. However, facial expressions are not unfailingly universal. Although some degree of agreement is generally evident across cultures, researchers have repeatedly found isolated groups whose identifications of the emotions from facial expressions, such as those for surprise and disgust, did not fully agree with those of Westerners (FIGURE 11.8), suggesting that different cultures have adopted different ways to express some of the emotions (Crivelli et al., 2016). These subtle cultural differences suggest that cultures prescribe rules for facial expression and that they control and enforce those rules by cultural conditioning. Everyone agrees that cultures affect the facial display of emotion; the remaining controversy is over the extent of that cultural influence (FIGURE 11.9). Facial expressions are mediated by muscles, cranial nerves, and CNS pathways The human face is a complicated object, a network of small muscles that are carefully controlled by the nervous system. We use subsets of those muscles to produce nuanced facial expressions, from grimace to grin, alongside less subtle facial behaviors, like eating and speaking. Facial muscles can be divided into two categories: 1. Superficial facial muscles mostly attach only between different points of facial skin (FIGURE 11.10), so when they contract, they change the shape of the mouth, eyes, or nose or maybe create a dimple. Watson/Breedlove The M2i.ndD'seMepacfahciniael muscles attach to bone and produce FoundatiolnasrogfeBrr-asincaalnedmBeohavveiomr 4eents, like chewing. MM4e_11.09 05/27/20 These facial muscles are innervated by two cranial nerves: (1) the facial nerve (VII), which innervates the superficial muscles of facial expression; and (2) the motor branch of the trigeminal nerve (V), which innervates muscles that move the jaw (see Figure 1.7). The activity of the cranial nerves is governed by the face area of motor cortex: a disproportionately large brain region in humans (see Figure 5.10), probably reflecting the importance of emotional expression in our species. An intriguing but controversial proposal--the facial feedback hypothesis--suggests that sensory feedback from our facial expressions can affect our mood, consistent with the James-Lange notion that sensations from our body inform us about our
FIGURE 11.10 Superficial Facial Muscles and Their Neural Control
Branches of the facial nerve: Temporal Zygomatic The facial nerve (VII) innervates the super cial muscles that contribute to emotional expression. Buccal Deep facial muscles, like those controlling the jaw, are innervated by the trigeminal nerve (V; not shown). Mandibular
emotions. So, for example, people who have been simulating a smile (by holding a pencil between their teeth) reportedly experience more positive feelings than participants who have been simulating a frown (Davis et al., 2009). Important questions have arisen about the strength and reliability of this finding (Wagenmakers et al., 2016), but if further study confirms that forcing yourself to smile may actually help you feel happier, then the old song that tells us to "just put on a happy face" may be sound advice. Being forced to display false emotional expressions in stressful situations, however, may have negative consequences for well-being and job happiness (Hülsheger and Schewe, 2011). 1. Compare and contrast the commonsense view of bodily responses to emotions with the James-Lange theory. 2. What two findings cast doubt on the James-Lange theory of emotions? 3. Describe the results of Schachter and Singer's experiment. What do these findings suggest about how autonomic reactions, emotional experience, and cognitive processing are related? 4. List some examples of particular facial expressions that are associated with particular emotions. 5. What is the evidence that emotions, and the facial expressions that accompany them, evolved by natural selection? 6. What evidence suggests that facial expressions of emotional state are inherited rather than taught by culture?
11.2Do Distinct Brain Circuits Mediate Different Emotions?
brain self-stimulation The process in which animals will work to provide electrical stimulation to particular brain sites, presumably because the experience is very rewarding. medial forebrain bundle A collection of axons traveling in the midline region of the forebrain. nucleus accumbens A region of the forebrain that receives dopaminergic innervation from the ventral tegmental area, often associated with reward and pleasurable sensations.
Next we consider neural systems implicated in the experience and expression of emotions, and brain mechanisms involved in emotional learning. After studying this section, you should be able to: 11.2.1 Define and describe the phenomenon of brain self-stimulation. 11.2.2 Sketch and describe the major brain mechanisms involved in emotional behaviors, noting the behavioral manifestations of activity in the major pathways. 11.2.3 Describe the process of fear conditioning, the neural mechanisms responsible for fear reactions, and the role of this system in pathological states. Studies that ask whether different emotions have their own distinct neural mechanisms have confirmed not only that some brain regions do specialize in emotions, but also that the same regions may be involved in multiple emotions. One way to study the neuroanatomy of emotion is to electrically stimulate brain sites in conscious animals and then observe the effects on behavior. Classic work in the 1950s produced an intriguing finding: rats will enthusiastically press a lever in order to give themselves brief electrical stimulation in a brain region called the septum (FIGURE 11.11) (Olds and Milner, 1954). This phenomenon, called brain self-stimulation, can also happen in humans. People receiving electrical stimulation in the septum feel a sense of pleasure or warmth, or sometimes sexual excitement (Heath, 1972). Building on the discovery of self-stimulation, a rush of experimentation soon mapped brain sites that support self-stimulation responses. Almost all of these sites are subcortical and are especially concentrated in a large axon tract that ascends from the midbrain through the hypothalamus: the medial forebrain bundle. An important destination for the axons of the medial forebrain bundle is the nucleus accumbens, a major
Animals will work very hard pressing a bar to receive mild electrical stimulation at any of the sites indicated here by large, red circles.
Basal forebrain Nucleus accumbens Medial forebrain bundle
FIGURE 11.11 Self-Stimulation Sites in the Rodent Brain
The ventral tegmental area (green) sends dopaminergic axons to the nucleus accumbens.
component of the brain's reward circuitry (see Figure 11.11 and Chapter 3). The release of dopamine into the nucleus accumbens appears to produce very pleasurable feelings. One theory is that the electrical stimulation taps into dopaminergic circuits that are normally activated by behaviors that produce pleasurable feelings, such as feeding or sexual activity (White and Milner, 1992). As we discussed in Chapter 3, researchers have proposed that drugs of abuse are addictive because they activate these same neural circuits with an artificial intensity (E. L. Gardner, 2011).
decorticate rage Also called sham rage. Sudden intense rage characterized by actions (such as snarling and biting in dogs) that lack clear direction. limbic system A loosely defined, widespread group of brain nuclei that innervate each other to form a network. These nuclei are implicated in emotions.
Klüver-Bucy syndrome A condition, brought about by bilateral amygdala
Early in the twentieth century, dogs in which the cortex had been removed were found
damage, that is characterized by dramatic
to respond to routine handling with sudden intense decorticate rage--snarling, biting, and so on--sometimes referred to as sham rage because it seemed undirect-
emotional changes including reduction in fear and anxiety.
ed. Clearly, then, emotional behaviors of this type must be organized at a subcorti-
cal level, with the cerebral cortex normally inhibiting rage responses. On the basis
of studies such as these, combined with observations
from brain autopsies of people with emotional disorders, James Papez (1937) proposed a subcortical circuit of emotion. Papez (whose name rhymes with "capes")
FIGURE 11.12 The Limbic System: Medial Brain Regions Involved in Emotions
noted associations between emotional changes and
specific sites of brain damage. These interconnected Watsroeng/iBorneesd, lnoovew known as the limbic system (MacLean, The Mind's Machine Foun1d9at4io9n)s, oinf Bcrlauidn eantdhBeehmavaiomr 4me illary bodies of the hypothalamus, the anterior thalamus, the cingulate cortex, the MM4hei_p1p1.o1c1am05p/u2s7,/t2h0 e amygdala, and the fornix. The ar-
rows in FIGURE 11.12 schematically depict the inter-
Early support for the limbic model of emotion came
from studies of monkeys after removal of their tempo-
ral lobes (Klüver and Bucy, 1938). The animals' behavior changed dramatically following surgery; the high-
light of this behavioral change was an extraordinary taming effect known as the Klüver-Bucy syndrome.
Animals that had been wild and fearful of humans before surgery became tame and showed neither fear
nor aggression afterward. They also showed strong
oral tendencies, eating a variety of objects, including
rocks! Frequent and often inappropriate sexual behavior was also observed. Because this type of behavior is
also seen in monkeys in which only the left and right
amygdalas have been destroyed--without damaging
any adjacent tissue (Emery et al., 2001)--it appears that
Amygdala Hippocampus Parahippocampal gyrus
fear conditioning A form of classical conditioning in which a previously neutral stimulus is repeatedly paired with an unpleasant stimulus, like foot shock, until the previously neutral stimulus alone elicits the responses seen in fear. amygdala A group of nuclei in the medial anterior part of the temporal lobe.
the amygdala is a key structure in the behavioral changes in Klüver-Bucy syndrome, especially the loss of fear, as we see next. The amygdala is crucial for emotional learning There is nothing subtle about fear, and fear-provoking situations elicit similar behaviors from individuals of many different species. For example, it is very easy to reliably elicit fear by using classical conditioning, in which the person or animal is presented with a stimulus such as light or sound that is paired with a brief aversive stimulus such as mild electric shock (FIGURE 11.13A). After several such pairings, the sound or light by itself effectively elicits behaviors associated with fear, such as freezing in position, and autonomic signs like rapid heart rate and heavy breathing. Studies of such fear conditioning allowed researchers to develop a map of the neural circuitry of emotional learning, which revealed the amygdala to be a key structure (FIGURE 11.13B). Located at the anterior medial portion of each temporal lobe, the amygdala is composed of about a dozen different nuclei, each with a distinctive set of connections. Lesioning just the central nucleus of the amygdala in rats prevents blood pressure increases and freezing behavior in response to a conditioned fear stimulus. Subsequent research has confirmed that the amygdala is crucial not only for aversive conditioning but also appetitive learning: conditioned positive emotional reactions to attractive stimuli, such as to sex-related stimuli, or other pleasurable signals. In both cases, the amygdala is thought to help form associations between emotional responses and specific memories of stimuli that are stored elsewhere in the brain (Paton et al., 2006; Janak and Tye, 2015). On its way to the amygdala, sensory information about emotion-provoking stimuli reaches a fork in the road at the level of the thalamus (recall from Chapter 1 that the thalamus acts like a switchboard, directing sensory information to specific brain regions). A direct projection from the thalamus to the amygdala, nicknamed the "low road" for emotional responses in the original fear-conditioning studies (LeDoux, 1996), bypasses conscious processing and allows for immediate emotional reactions to stimuli (De Gelder et al., 2012; Celeghin et al., 2015). An alternate "high road" pathway routes the incoming information through sensory cortex, allowing for processing that, while slower, is conscious, fine-grained, and integrated with higher-level cognitive processes (FIGURE 11.13C). You can learn more details about the amygdala circuitry for fear and other emotions in A STEP FURTHER 11.1, on the website. Data from rats and mice about the role of the amygdala in fear mesh well with observations of humans. For example, when people are shown visual stimuli associated with pain or fear, fear-specific activity is observed in amygdala neurons (S. Wang et al., 2014), and activation of the amygdala may be observed even if the person is not consciously aware of the stimuli (Pegna et al., 2005). Similarly, when people view facial expressions of fear, electrophysiological responses occur much more quickly in the amygdala than in visual cortex, reflecting the privileged low-road access of the fear-inducing stimulus (Méndez-Bértolo et al., 2016). People who have temporal lobe seizures that include the amygdala commonly report that intense fear accompanies seizures (Engel, 1992; Chong et al., 2016), and electrical stimulation of temporal lobe sites during brain surgery likewise may elicit feelings of fear (Nowacki et al., 2015). In a rare condition called Capgras delusion, people believe that their significant others have been replaced by impostors; although it is more typically a psychiatric symptom, some cases of Capgras delusion are thought to result from brain damage that robs the afflicted person of the privileged low-road connection between visual stimuli (like faces) and the emotions they would normally elicit (Ellis and Lewis, 2001). The neural mechanisms of fear conditioning are also thought to play a central role in post-traumatic stress disorder (PTSD; see Chapter 12), in which memories of horrible events repeatedly intrude into consciousness, reawakening all the autonomic and psychological symptoms of fear.
In one classical-conditioning procedure, called fear conditioning, a tone is associated with a mild electrical shock, which causes increased blood pressure and "freezing." (A)
Eventually the tone alone elicits these responses.
Blood pressure (mm of mercury) Duration of freezing (s) Blood pressure Duration of freezing (s) "Hig Blood pressure Duration of freezing (s)
Hippocampus Amygdala A fear-inducing stimulus reaches the thalamus and is relayed either directly to the amygdala (the "low road" for unconscious reactions to threat) or via the cortex and hippocampus (the "high road," involving more detailed and conscious processing of stimuli).
FIGURE 11.13 The Circuitry of Fear (Parts A and B after
J. E. LeDoux, 1994. Sci. Am. 270: 50; C after J. E. LeDoux,
1996. The emotional brain: The mysterious underpinnings
The information ultimately reaches the amygdala's central nucleus, which projects to different brain nuclei to produce different components of the fear response.
Emotional Autonomic Hormonal behavior responses responses
View Activity 11.1: Conditioned Fear Response
FIGURE 11.14 The Woman Who Was Never Afraid (After J. S. Feinstein et al., 2011. Curr. Biol. 21: 34.)
Most people who watch these lm clips report afterward that they felt afraid.
However, patient S.M. reported little or no fear. Note that what little arousal she reports to various lms does not match well with other people's rating of how scary those clips are.
A - The Ring (2002) The ghost of a murdered child in ltrates the lives of her soon-to-be victims. B - Blair Witch Project (1999) Campers are attacked by an unknown apparition during the middle of the night. C - CSI (2009) A man struggles to survive after being buried alive. D - The English Patient (1996) A man is tortured by the Germans during World War II. E - Se7en (1995) A mutilated man awakes from the dead. F - Cry Freedom (1987) Armed trespassers attack a woman who is home alone during the night. G - Arachnophobia (1990) A large poisonous spider attacks a girl in the shower. H - Halloween (1978) A woman is being chased by a murderer. I - The Shining (1980) A young boy hears voices in the hallway of a haunted hotel. J - The Silence of the Lambs (1991) A female FBI agent tries to capture a twisted serial killer who is hiding in a dark basement.
But perhaps the most compelling evidence that the amygdala is important for fear in our species comes from people like patient S.M., the woman we met at the start of the chapter, who is literally fearless. The fearlessness that she and other people with the disorder display seems almost certainly due to the loss of the amygdala. Her very rare genetic condition causes the accumulation of calcium deposits in the amygdala, starting in late childhood, which eventually destroys the nuclei in both cerebral hemispheres. When S.M. is shown movie clips that other people find frightening, she reports being unmoved (FIGURE 11.14). S.M. is also very poor at recognizing the facial expressions of fear in other people, but she recognizes other emotional expressions--a pattern seen in other people with damaged amygdalas (Adolphs et al., 2005). Interestingly, when S.M. Watson/Breedlove The Mwiansd'assMkeadchtionebreathe air with a high concentration of carbon dioxide, she soon felt a panFoundicaktiyonfseoafrB, rfalianilainndgBhehearvhioar n4eds about (Feinstein et al., 2013). This result suggests that some other brain system mediates the fear of internal threats, such as a lack of oxygen. MM4e_11.14 09/04/20 Different emotions activate different regions of the human brain Several forebrain areas are consistently implicated in varying emotions. Bartels and Zeki (2000) recruited volunteers who professed to be "truly, deeply, and madly in love." Each participant furnished four color photographs: one photo of their romantic partner, and three photos of friends who were of the same gender as the loved partner and who were similar in age and length of friendship. Functional-MRI brain scans were made while each participant was shown counterbalanced sequences of the four photographs. Brain activity elicited by viewing the loved person was compared with that elicited by viewing friends. Love, compared with friendship, involved increased
Brain regions implicated in emotions are depicted here in midsagittal...
of prefrontal cortex cingulate cortex cingulate cortex
Orbitofrontal region of prefrontal cortex
...and posterior coronal sections. Different emotions are associated with varying patterns of activity across emotion-related brain regions.
All images from R. J. Dolan, 2002. Science 298: 1191
activity in the insula and anterior cingulate cortex and reduced activity in the posterior cingulate and prefrontal cortices (FIGURE 11.15). Given its role in fear, you won't be surprised to learn that the amygdala also showed reduced activity when people were contemplating their romantic partners. Activity of the anterior insular cortex (see Figure 3.16) has been implicated in our conscious experience of these varied and nuanced emotional states; impairments in emotional awareness, termed alexithymia, are associated with dysfunction of the insula (Gu et al., 2013). Another study compared brain activation during four different kinds of emotion, and again the insula, cingulate cortex, and prefrontal cortex were among the regions implicated. These studies indicate that there is no simple, one-to-one relation between a specific emotion and changed activity of a brain region. There is no "happy center" or "sad center." Instead, each emotion involves differential patterns of activation across a network of brain regions associated with emotion, as you can see in A STEP FURTHER 11.2, on the website. For example, activity of the cingulate cortex is altered in sadness, happiness, and anger, while the left somatosensory cortex is deactivated in both anger and fear. Although different emotions are associated with different patterns of activation, there is a good deal of overlap among patterns for different emo- Watson/Breedlove The Mtiionnds's(MAa.cRh.inDeamasio et al., 2000). FoundatioLnseotf'sBfroaicnuasndnBeexhtavoionr t4he e darker side of human emotional behavior--the forms and causes of aggression--before we turn our attention to stress and the toll these nega- MM4e_11.15 05/27/20 tive experiences take on our health.
1. Describe brain self-stimulation and what this phenomenon suggests about emotional experience. 2. What is the limbic system, and what happens when portions of this system are damaged, such as in Klüver-Bucy syndrome? 3. Describe fear conditioning and the evidence that the amygdala plays a role in this process. 4. What evidence suggests that the amygdala mediates fear in humans?
11.3Neural Circuitry, Hormones, and Synaptic Transmitters Mediate Violence and Aggression
Next we sharpen our focus on the neural and hormonal bases of violence and other aggressive behaviors. By the end of this section, you should be able to: 11.3.1 Define and distinguish between multiple forms of aggression. 11.3.2 Summarize research on the role of testosterone in aggression, contrasting between humans and nonhuman animals. 11.3.3 Identify the key neural systems implicated in aggression and the environmental stimuli that activate these systems. 11.3.4 Discuss the biopsychological origins of violent behavior in humans, and speculate about targets for reducing violent behavior.
aggression Behavior that is intended to cause pain or harm to others. intermale aggression Aggression between males of the same species. testosterone A hormone, produced by male gonads, that controls a variety of bodily changes that become visible at puberty; one of a class of hormones called androgens. Nature, Red in Tooth and Flipper Fighting male elephant seals draw blood. In most mammalian species, males must compete with one another, often in the form of physical aggression, for the chance to mate with females.
Violence, assaults, and homicide exact a high price in modern society, and physical assault is not the only form of aggression. Verbal and symbolic aggression--name calling, horn honking, angry glares--also take their toll. We can define aggression as behavior that is intended to cause pain or harm (whether physical or emotional) to others, either individually or in groups. We will focus primarily on physical aggression between individuals, excluding the aggression of predators toward their prey, which is better viewed as feeding behavior (Glickman, 1977). Intermale aggression (aggression between males of the same species) is observed in most vertebrates. The relevance to humans is reflected in the fact that males are 5 times as likely as females to be arrested on charges of murder in the United States. Whatever we may think about aggression, it seems clear that in many species aggressive behavior in males is adaptive for gaining access to food and mates. In the wild, groups of male chimpanzees sometimes band together to kill a rival male (Wilson et al., 2014), increasing the attackers' chances of mating in the future. In the USA in 2018, about 75% of people arrested for assault were male, and almost 90% of murder arrests involved male offenders (FBI, 2018). Aggressive behavior between boys, in contrast to that between girls, is evident early in life, in the form of vigorous and destructive play behavior (J. Archer, 2006). These and similar observations suggest that the hormone that prepares males for reproduction--testosterone--also plays a role in their aggressive behavior. Androgens seem to increase aggression At sexual maturity, as the testes begin secreting the steroid hormone testosterone, intermale aggression markedly increases in many species (Svare, 2013). In seasonally breeding animals as diverse as birds and primates, intermale aggression waxes and wanes in concert with seasonal changes in levels of testosterone (Bronsard and Bartolomei, 2013; Munley et al., 2018). Conversely, castrating males to remove the source of testosterone usually reduces aggressive behavior profoundly. Treating castrated males with testosterone restores fighting behavior (FIGURE 11.16). The relationship between testosterone and aggression in humans is more complicated (for a review, see Geniole and Carré, 2018). Treating adult volunteers with extra testosterone does not increase their aggression (O'Connor et al., 2004). Similarly, young men going through puberty experience a sudden large increase in circulating testosterone, yet they do not show a correlated increase in aggressive behavior (J. Archer, 2006). Nevertheless, some human studies report that testosterone levels correlate with hostility, as measured by behavior rating scales, and are also associated with unprovoked versus defensive violence in both men and women (Denson et al., 2018). At least two variables confound the correlations between testosterone and aggression. First is the observation that experience can affect testosterone levels. In mice and monkeys, the loser in aggressive encounters shows reduced androgen levels (Lloyd, 1971; I. S. Bernstein and Gordon, 1974), so measured levels of testosterone sometimes may be a result, rather than a cause, of behavior. In men, testosterone levels rise in
Males are signi cantly more aggressive before castration than afterward.
Females show little aggression, and removal of the ovaries has no effect on this behavior.
Testosterone treatment of castrated males reinstates aggression for as long as the hormone is supplied.
FIGURE 11.16 The Effects of Androgens on the Aggressive Behavior of Mice (After G. C. Wagner et al., 1980. Aggress. Behav. 6: 1.)
the winners and fall in the losers after competitions ranging from wrestling to chess (van Anders and Watson, 2006). Male sports fans even show a vicarious testosterone response to simply watching "their" team participate in sporting events (Van der Meij et al., 2012); in some studies the degree of the vicarious hormonal response relates to whether the team wins or loses (Bernhardt et al., 1998). During the 2008 U.S. presidential election, men who voted for John McCain experienced a sharp drop in circulating testosterone, compared with backers of Obama, who won (Stanton et al., 2009). These observations suggest that a second confounding variable between testosterone and aggression is dominance (Mazur and Booth, 1998). According to this model, testosterone levels should be associated with behaviors that confer or protect the individual's social status (and thus reproductive fitness). This type of aggression is said to be proactive: part of an offense strategy to improve the individual's standing in comparison to others or achieve a desired social outcome. In contrast, reactive aggression encompasses the many forms of defensive behavior, ranging from freezing Watstoonp/rBereeemdlpotvieve attacks, that protect against external threats (Wrangham, 2018; LeDoux The ManinddD's aMwac,h2i0n1e8). Despite the lack of a close relationship between aggression and an- Foundations of Brain and Behavior 4e drogens, people have tried to modify the behavior of male criminals by manipulating MMs4ee_x11h.o16rmo09n/e0s1,/t2h0rough surgical castration or "chemical" castration with drugs that block androgen receptors or testosterone production. While lowered testosterone may reduce violence in some sex offenders (L. E. Weinberger et al., 2005), the main effect is a reduction in sexual motivation more than a direct effect on aggression. Many ethical issues raised by this approach to the rehabilitation of sex offenders, not to mention the intricacies of such intervention, have yet to be worked out. Brain circuits mediate aggression Aggressive behavior in various animals, including humans, is modulated by brain activity associated with several neurotransmitter systems, including dopamine, GABA, vasopressin, and especially serotonin (Numan, 2015; Rosell and Siever, 2015). For example, Higley et al. (1992) observed aggressive behavior in 28 monkeys from a large,
medial amygdala A portion of the amygdala that receives olfactory and pheromonal information. ventromedial hypothalamus (VMH) A hypothalamic region involved in sexual behaviors, eating, and aggression. maternal aggression Aggression of a mother defending her nest or offspring. psychopath An individual incapable of experiencing remorse. Psychopathic Impulsivity Serial killer Ted Bundy displayed many characteristics of a psychopath. He was superficially charming and, as shown here acting out in the courtroom when the judge was away, impulsive in nature. This scene also hints that, like other psychopaths, Bundy felt little or no remorse for his actions.
free-ranging colony, and they ranked the animals from least to most aggressive. When researchers gauged serotonin activity by measuring serotonin metabolites in the cerebrospinal fluid, they found evidence that the most aggressive monkeys had the lowest levels of serotonin being released in the brain. Similarly, genetically modified mice that lack a specific subtype of serotonin receptor are hyperaggressive (Bouwknecht et al., 2001)--just what we would expect if serotonin normally inhibits aggression. This inhibitory role of serotonin in aggression is probably evolutionarily ancient, since it is evident even in invertebrates like crayfish and locusts (Panksepp et al., 2003; Anstey et al., 2009). Drugs that enhance GABA transmission generally reduce aggressive behavior in humans (Lieving et al., 2008), although, paradoxically, these drugs--for example, benzodiazepine agonists and alcohol--occasionally provoke aggression in a minority of users (Albrecht et al., 2016; Guina and Merrill, 2018). The medial amygdala analyzes olfactory and pheromonal information, allowing male rats and mice to distinguish between male rivals to be attacked and females to be courted. That information is relayed to the ventromedial hypothalamus (VMH), which serves as a trigger to activate aggressive behavior. In optogenetic experiments--the use of light to activate neurons in genetically modified mice--activation of VMH neurons can cause males that have been mating with females to suddenly attack them (H. Lee et al., 2014). Conversely, using optogenetic techniques to instead inhibit VMH activity reduces the likelihood of attack (Falkner et al., 2016). And a direct input to the VMH from the suprachiasmatic nucleus--the brain's circadian clock (see Chapter 10)--appears to regulate the daily variation in aggression seen in many species, including our own (Todd et al., 2018). So far we've discussed aggression in males, but females are also aggressive at times, particularly when they are caring for their young. This maternal aggression is typically studied by introducing an intruder mouse, usually a male, into the cage of a mother nursing a litter. In such conditions, she may immediately attack the intruder. Maternal aggression, like male aggression, is controlled by neural circuits in the VMH, as well as other regions, including the preoptic area (POA), the premammillary nucleus (Motta et al., 2013), and a serotonergic projection originating from the midbrain (Holschbach et al., 2018). The biopsychology of human violence is a controversial topic Some forms of human violence are characterized by sudden, intense physical assaults. A long-standing controversy surrounds the idea that some forms of intense human violence are caused by temporal lobe disorders (Mark and Ervin, 1970). Aggression is sometimes a prominent symptom in people with temporal lobe seizures, and a significant percentage of people arrested for violent crimes have abnormal EEGs or other indicators of temporal lobe dysfunction (Cope et al., 2014). Psychopathy is not a psychiatric disorder with formal diagnostic criteria in the DSM-5--instead it describes a cluster of personality traits that may be associated with antisocial behaviors. Psychopaths are often intelligent individuals with superficial charm who have poor self-control, a grandiose sense of self-worth, and little or no feelings of remorse (Hare et al., 1990). And while most people who score high on psychopathic tendencies lead normal, often highly successful lives, psychopaths have sometimes committed horribly violent acts without compunction. Compared with controls, psychopaths do not react as negatively to words about violence (N. S. Gray et al., 2003), and they show blunted responses to aversive cues associated with fear conditioning that typically cause strong reactions in other people (Glenn and Raine, 2014). Imaging studies suggest that psychopaths have reductions in both the size and activity of prefrontal cortex (FIGURE 11.17), which may impair their ability to control impulsive behavior (Yang et al., 2012; 2015). Undoubtedly, human violence and aggression stem from many sources. Biological studies of aggression have been vigorously criticized by some politicians and social scientists. These critics argue that, as a result of emphasizing biological factors such as genetics or brain mechanisms, the preventable origins of human violence and aggression, such as poverty and child neglect, might be overlooked. But as we have seen throughout
© Bill Frakes/Time and Life Pictures/Getty Images
FIGURE 11.17 Brain Abnormalities in Psychopaths (After M. Ly et al., 2012. Am. J. Psychiatry 169: 743.)
Hot colors (red/yellow) indicate areas of cortical thinning in incarcerated psychopaths, relative to non-psychopathic inmates. Thinning is especially evident in left frontal cortex, and bilateral temporal and cingulate cortex. Medial view
the book, the brain is a malleable organ that is shaped by experience--and violent behavior must have its origins in the brain--so in principle it could be possible to reshape or at least moderate brain mechanisms of violence. The quality of life of some violent persons might be significantly improved if biological problems could be identified and addressed. For example, treatments that enhance serotonin activity in the brain might be a useful adjunct to psychotherapeutic intervention (George et al., 2011). Next, let's look at one of the principal consequences of aggression and other aversive situations: stress. 1. Why is intermale aggression common in so many species? 2. What is the relationship between androgens and aggression? 3. Which neurotransmitter has been most consistently implicated in aggression? Watson/Breedlove The 1Mi1nd.'4s MaSchtirneess Activates Many Bodily Responses Foundations of Brain and Behavior 4e MM4e_11.17 05/27/20 We conclude the chapter by looking at the ways in which reciprocal connections between the nervous system, the endocrine system, and the immune system allow them to regulate each other to preserve our health. By the end of this section, you should be able to: 11.4.1 Summarize the physiological correlates of stress, and contrast acute and chronic stress responses. 11.4.2 Discuss the ways in which people differ in their vulnerability and responses to stressful situations, and give examples of how early life experiences affect these individual differences. 11.4.3 Describe the communication between the nervous system and the immune system and how brain responses to stress can affect health. 11.4.4 Summarize the impact of chronic stress on health, as well as possible ways to mitigate these effects.
stress Any circumstance that upsets homeostatic balance. adrenal medulla The inner core of the adrenal gland. epinephrine Also called adrenaline. A compound that acts both as a hormone (secreted by the adrenal medulla under the control of the sympathetic nervous system) and as a synaptic transmitter. norepinephrine Also called noradrenaline. A neurotransmitter produced and released by sympathetic postganglionic neurons to accelerate organ activity. adrenal cortex The steroid-secreting outer rind of the adrenal gland. adrenal corticosteroid hormone A steroid hormone that is secreted by the adrenal cortex. cortisol A glucocorticoid stress hormone of the adrenal cortex.
We all experience stress, but what is it? Attempts to define this term have a certain vagueness. Hans Selye (1907-1982), whose work launched the modern field of stress research, broadly defined stress as "the rate of all the wear and tear caused by life" (Selye, 1956). Nowadays, researchers try to sharpen their focus by treating stress as a multidimensional concept that encompasses stressful stimuli, the stress-processing system (including cognitive assessment of the stimuli), and responses to stress. While many different parts of the body respond to stress, it's clear that the brain carefully monitors and controls those responses (McEwen et al., 2015). The stress response progresses in stages Selye called the initial response to stress the alarm reaction. As one part of the alarm reaction, the hypothalamus activates the sympathetic nervous system to ready the body for action; this is the fight-or-flight system we mentioned at the start of the chapter. The sympathetic system stimulates the core of the adrenal gland, which is called the adrenal medulla, to release the hormones epinephrine (also known as adrenaline) and norepinephrine (or noradrenaline). These hormones act on many parts of the body to boost heart rate, breathing, and other physiological processes that prepare the body for action. As another part of the alarm reaction, the hypothalamus stimulates the anterior pituitary to release a hormone that drives the outer layer of the adrenal gland, the adrenal cortex. Activation of this hypothalamic-pituitary-adrenal axis (HPA axis) results in the release of adrenal corticosteroid hormones such as cortisol (FIGURE 11.18). These hormones act more slowly than epinephrine, but they also ready the body for action, including releasing body stores of energy. Glucocorticoid receptors--the receptors that respond to cortisol--are found in many locations in the brain, where they are thought to mediate the formation of memories associated with stress and fear (De Quervain et al., 2017), as well as regulating the ongoing secretion of stress hormones via negative feedback (see Figure 8.11).
(A) Sympathetic nervous system: epinephrine
(B) Hypothalamic-pituitary-adrenal axis: cortisol
1 In response to stress, the hypothalamus activates the sympathetic nervous system to stimulate many physiological systems... 2 ...including the adrenal medulla (the core of the adrenal gland) to release the hormones epinephrine and norepinephrine.
Hypothalamus Anterior pituitary 3 The hypothalamus also stimulates the anterior pituitary to release hormones that drive the outer part of the adrenal gland, the adrenal cortex, to release steroids such as cortisol.
FIGURE 11.18 Physiological Reactions to Stress
Epinephrine Cortisol Norepinephrine Stress response
4 All these hormones prepare the body for action.
(A) Response systems affected in jump situation Heart Liver
FIGURE 11.19 Autonomic Activation during a Stress Situation (B after H. Ursin et al., 1978. Psychobiology of stress: A study of coping men. Academic Press. New York, NY.)
Hormonal responses Parasympathetic responses Sympathetic responses
(B) Hormonal responses Cortisol (µg/100 mL)
In classic research, hormonal responses to stress were studied in a group of young recruits in the Norwegian military both before and during scary parachute training (Ursin et al., 1978). On each jump day, the anterior pituitary released enhanced levels of hormones, and both the sympathetic and parasympathetic systems were activated (FIGURE 11.19A). Initially, cortisol levels were elevated in the blood before each jump, but with more and more successful jumps over successive days, the pituitary-adrenal response soon declined. Epinephrine and norepinephrine were also elevated before the first jumps, but eventually they returned to normal before jumps. Testosterone showed the reverse pattern, falling far below control levels on the first day of training but returning to normal with subsequent jumps (FIGURE 11.19B). Once the soldiers mastered the jumps, they no longer showed increased hormonal responses, having adapted to the activity. Less-dramatic real-life situations also evoke clear endocrine responses (FranWatskoenn/Bhraeeedulsoevre, 1978). For example, riding in a commuter train provokes the release of The Mepinind'espMharcihnien;ethe longer the ride and the more crowded the train, the greater the horFounmdatoionnas lofrBersapinoannsdeB(eFhaIGvioUrR4eE 11.20A). Factory work likewise leads to the release of epiMM4nee_p11h.1r9ine;08t/h2e4/sh20orter the work cycle--that is, the more frequently the person has to repeat the same operations--the higher the levels of epinephrine. The stress of a PhD oral exam leads to a dramatic increase in both epinephrine and norepinephrine (FIGURE 11.20B), and medical students stressed by preparing for their licensing exams
Before training (baseline) Before that day's jump After that day's jump
Increase of epinephrine during journey (% of control level) Hormone secretion (picomoles/ minute)
FIGURE 11.20 Hormonal Changes in Humans in Response to Social Stresses (A after U. Lundberg, 1976. J. Human Stress 2: 26; B after M. Frankenhaeuser, 1978. Nebr. Symp. Motiv. 26: 123, edited by Richard A. Dienstbier by permission of the University of Nebraska Press. Copyright 1978 by the University of Nebraska Press.)
A small, 10% increase in the number of commuter train passengers during a period of gasoline rationing resulted in a much higher level of epinephrine secretion.
Levels of epinephrine and norepinephrine in a graduate student during a 2-week period before, during, and after a PhD thesis oral examination re ect levels of stress. (B)
showed fMRI evidence of impairments in the brain mechanisms controlling attention; following the exam, their fMRI scans returned to normal (Liston et al., 2009). Sustained social stressors can also exact lasting medical costs: for example, young people with asthma who experience stress due to peer rejection or family conflict have a more responsive adrenal system, more severe respiratory symptoms, and impaired expression of anti-inflammatory genes (Murphy et al., 2015; Farrell et al., 2018). In general, childhood stress has an enduring impact on health in later life, including neural and cognitive development, emotional regulation, and measures of lifetime achievement (Cameron et al., 2017; see Chapter 4). There are individual differences in the stress response Why do individuals differ in their responses to stress (Infurna and Luthar, 2016)? One hypothesis focuses on early experience. Rat pups clearly find it stressful to have a human pick them up and handle them. Yet rats that have been briefly handled as pups are less susceptible to adult stress than are rats that have been left alone as pups Watso(nS/.BLreeevdilnoeveet al., 1967). For example, the previously handled rats secrete lower adrenal The Msitnedr'os iMdaacmhinoeunts in response to a wide variety of adult stressors. Researchers termed Foundations of Brain and Behavior 4e this effect stress immunization because a little stress early in life seemed to make the MM4ea_n1i1m.20als 0m9/o0r1e/r2e0silient to later stress. Follow-up research showed that there was more to the story. The pups did not benefit because they were stressed; they benefited because their mothers comforted them after the stress. When pups are returned to their mother after a separation, she spends considerable time licking and grooming them. And she will lick the pups much longer if they were handled by humans during the separation. Michael Meaney and colleagues suggest that this gentle tactile stimulation from Mom is crucial for the stress immunization effect. They found that, even among undisturbed litters, the offspring of mother rats that exhibited more licking and grooming behavior were more resilient in their responses to adult stress than other rats were (D. Liu et al., 1997). So the "immunizing" benefit of early stressful experience happens only if the pups are promptly comforted after each stressful event. If the pups are deprived of their mother for long periods, receiving very little of her attention, then as adults they exhibit a greater stress response, have difficulty learning
mazes, and show reduced neurogenesis in the hippocampus (Mirescu et al., 2004). Maternal deprivation exerts this negative effect on adult stress responses by causing long-lasting changes in the expression of adrenal steroid receptors in the brain. This change is termed epigenetic regulation because it represents a change in the expression of the gene, rather than a change in the encoding region of the gene (see Figure 4.14 and Figure 4.15). Dramatic evidence for the same phenomenon has been seen in humans. For example, examination of the brains of suicide victims revealed the same epigenetic change in expression of the adrenal steroid receptor, but only in those victims who had a history of being abused or neglected as children (McGowan et al., 2009). The implication is that the early abuse epigenetically modified expression of the gene, making the person less able to handle stress and thus more likely to develop significant psychiatric disturbances--especially mood and anxiety disorders--that heighten the risk of suicide. Suicide victims who had no history of early neglect did not show the epigenetic change, so their suicidality may have been the result of mental health issues of different origin. Stress and emotions affect our health The field of psychosomatic medicine studies the distinctive psychological, behavioral, and social factors that influence individual susceptibility or resistance to diverse illnesses. The related field called health psychology (or behavioral medicine) emphasizes the role of social factors in the cause, progression, and consequences of health and illness (Ogden, 2012). For example, an active area of research is concerned with the association between heart disease and behavioral and social factors such as hostility, depression, loneliness, and stress at home and at work (Matthews, 2005; Rozanski, 2014). The field of psychoneuroimmunology studies how the immune system--with its collection of cells that recognize and attack intruders--interacts with other organs, especially those of the hormonal systems and nervous system (Ader, 2001). Studies of both human and nonhuman subjects clearly show psychological and neurological influences on the immune system. For example, people with happy social lives are less likely to develop a cold when exposed to the virus (S. Cohen et al., 2006). People exposed to a cold virus have more severe symptoms if they are experiencing conflict with others. But individuals who feel they have more social support, and who receive more hugs from others, are protected from that effect of conflict (S. Cohen et al., 2015). Likewise, people who tend to feel positive emotions will also produce more antibodies in response to a flu vaccination (Rosenkranz et al., 2003), which should help them fight off sickness. These interactions go both ways: the brain influences responses of the immune system, and immune cells and their products affect brain activities, as FIGURE 11.21 shows. You can learn details of how the immune system, endocrine system, and nervous system communicate with one another in A STEP FURTHER 11.3, on the website. Periods of elevated stress--such as exam periods and pandemics!--frequently suppress the immune system. For students taking exams, individual perceptions of the stress of the academic program predict the degree of immune system suppression: those who perceive the program as stressful show the most suppression (Glaser and Kiecolt-Glaser, 2005). One experiment considered the effects of university examinations on wound healing in dental students (Marucha et al., 1998). Two small wounds were placed on the roof of the mouth of 11 dental students (sounds like revenge, doesn't it?). The first wound was timed during summer vacation; the second was inflicted 3 days before the first major examination of the term. Two independent daily measures showed that no student healed as rapidly during the exam period, when healing took 40% longer. One measure of immunological response declined 68% during the exam period. The experimenters concluded that even something as transient, predictable, and relatively benign as final exams (do students agree with this description?) can significantly impede wound healing.
epigenetic regulation Changes in gene expression that are due to environmental effects rather than to changes in the nucleotide sequence of the gene. psychosomatic medicine A field of study that emphasizes the role of psychological factors in disease. health psychology Also called behavioral medicine. A field of study that focuses on psychological influences on health-related processes. psychoneuroimmunology The study of the immune system and its interaction with the nervous system and behavior.
Nervous system, memory and perception, coping/appraisal strategies
FIGURE 11.21 Factors That Interact during the Development and Progression of Disease
Long-Term Consequences of Childhood Bullying
There is growing recognition that children who are bullied, subjected to verbal or physical assault by other children, are at greater risk for mental and physical disorders when they grow up. A British study of children born in 1958 first gathered reports of whether they were being bullied at ages 7 and 11, then followed their health until they were age 50. After adjusting for IQ and other factors, the researchers found that those bullied as children were at increased risk for anxiety disorders and depression, as well as suicide (FIGURE 11.22) (Takizawa et al., 2014). Another study of both British and American children confirmed that those who were bullied were more likely to suffer these disorders. The authors were surprised to see that the effects of bullying were as strong as those of physical or sexual abuse (Lereya et al., 2015). Faced with such reports, schools are being encouraged to develop antibullying programs that teach children to recognize and report bullying and that train teachers to intervene rather than downplay bullying as a rite of passage or "normal" behavior. There is growing recognition many children today are subjected to another level of bullying--cyberbullying though social media (Hogan and Strasburger, 2020). Several
Percentage increased risk after controlling for other variables
FIGURE 11.22 Being Bullied Is Bad for Your Health (After R. Takizawa et al., 2014. Am. J. Psychiatry 171: 777.)
U.S. federal departments have collaborated to provide an online resource to increase understanding and combat bullying, including cyberbullying, at www.stopbullying.gov.
View Activity 11.2: The Stress Response and Consequences of Prolonged Stress
Why does chronic stress suppress the immune system?
Although brief stress doesn't impair immune function, and may even enhance it
(Dhabhar, 2018), longer-lasting stress has a pronounced suppressive effect on the im-
mune system. We discussed earlier how in response to stress, the brain causes adrenal
steroid hormones such as cortisol to be released from the adrenal cortex. In chronic stress,
these adrenal steroids directly suppress the immune system. But doesn't it seem like a
bad idea to suppress immunity just when you are more likely to sustain an injury, and
maybe an infection? Modern evolutionary theory offers some possible explanations for
this seemingly maladaptive situation (for a very readable account, see Sapolsky, 2004).
To the extent that stress might be a sudden emergency, the temporary suppression
of immune responses makes some sense because the stress response demands a rapid
mobilization of energy. Slow and long-lasting immune responses consume energy
that otherwise could be used for dealing with the emergency at hand. A zebra wound-
ed by a lion must first escape and hide, and only then does infection of the wound
pose a threatW. Satosotnh/eBsreteredslosvoef the encounter first suppresses the immune system, con-
serving resoTuhreceMsinudn'tsiMl aacshaifnee haven is found. Later the animal can afford to mobilize
of Brain and Behavior 4e heal the wound. The
(inflammatioMnM) o4ef_i1n1j.u22ries0,8e/s2p4/e2c0ially of joints, to help the animal remain mobile long
enough to find refuge (S. S. Cox et al., 2014). It is precisely this action that makes adre-
nal steroids like prednisone such useful medicines for treating inflammation.
In the wild, animals are under stress for only a short while; any animal stressed
for a prolonged period dies. So natural selection has favored stress reactions as a drastic
effort to deal with a short-term problem. What makes humans "special" is that, with
our highly social lives and keen analytical minds, we are capable of experiencing stress
for prolonged periods--months or even years. The bodily reactions to stress, which
TABLE 11.1 The Stress Response and Consequences of Prolonged Stress
Principal components of the stress response
Common pathological consequences of prolonged stress
Mobilization of energy at the cost of energy storage
Increased cardiovascular and cardiopulmonary tone
Psychogenic dwarfism, bone decalcification
Suppression of immunity and of inflammatory response
Neural responses, including altered cognition and sensory thresholds
Accelerated neural degeneration during aging
Source: R. M. Sapolsky, 2002, in J. B. Becker et al., (Eds.) Behavioral endocrinology (2nd. ed.). Cambridge, MA: MIT Press.
evolved to deal with short-term problems, become a handicap when extended too long (Sapolsky, 2004). TABLE 11.1 lists a variety of stress responses that are beneficial in the short term but detrimental in the long term. What we have described so far is a really depressing picture. If you are stressed for long periods of time, your health suffers, which brings another source of stress to your life. But don't give up hope. Even if there are some sources of stress you cannot avoid altogether, there are things you can do to reduce the impact of stress. Relaxation training involves focusing your attention on something calming while becoming more aware of your body, trying to relax muscles as much as you can (McGuigan and Lehrer, 2007). A program of therapy to deal with stress, partially inspired by various practices of meditation, is mindfulness-based stress reduction (MBSR). MBSR pairs relaxation with efforts to focus attention on the present moment, including current sensations, thoughts, and bodily states, in an open, nonjudgmental way. MBSR is focused on results and does not require practitioners to adopt any particular religious or spiritual views. It has been shown to reduce activity in the amygdala (Goldin and Gross, 2010) and prevent relapses of anxiety disorders or depression (Hofmann et al., 2010).
1. What are the hormonal responses to stressful events, and how do those change as individuals adapt to those events? 2. What is stress immunization, and how is it mediated by epigenetic events? 3. Why do we suppress the immune system in times of stress, and how does that suppression impair health in brainy, social animals like us? 4. In what ways is a childhood history of being bullied evident in the psychological health of adults? Recommended Reading Adolphs, R., and Anderson, D. J. (2018). The Neuroscience of Emotion: A New Synthesis. Princeton, NJ: Princeton University Press. Chen, A. (Ed.) (2019). Stress Resilience: Molecular and Behavioral Aspects. New York, NY: Academic Press. Davis, K. L., and Panksepp, J. (2018). The Emotional Foundations of Personality: A Neurobiological and Evolutionary Approach. New York, NY: W. W. Norton. Fernánadez-Dols, J.-M., and Russel, J. A. (Eds.) (2017). The Science of Facial Expression. New York, NY: Oxford University Press.
Fields, D. R. (2016). Why We Snap: Understanding the Rage Circuits in Your Brain. New York, NY: Dutton. Gross, J. J. (2015). Handbook of Emotion Regulation (2nd ed.). New York, NY: Guilford Press. Keltner, D., Oatley, K., and Jenkins, J. M. (2019). Understanding Emotions (4th ed.). New York, NY: Wiley. LeDoux, J. (2015). Anxious: Using the Brain to Understand and Treat Fear and Anxiety. New York, NY: Viking. Raine, A. (2013). The Anatomy of Violence: The Biological Roots of Crime. New York, NY: Pantheon. Sapolsky, R. (2004). Why Zebras Don't Get Ulcers (3rd ed.). New York, NY: Holt.
11 · VISUAL SUMMARY You should be able to relate each summary to the adjacent illustration, including structures and processes. The online version of this Visual Summary includes links to figures, animations, and activities that will help you consolidate the material.
1 Emotions are a constellation of feelings, behaviors, and physiological reactions. The James-Lange theory considered emotions to be the perceptions of stimulus-induced bodily changes. The Cannon-Bard theory emphasized simultaneous emotional experience and bodily response. In Schachter and Singer's cognitive theory, we attribute visceral arousal to specific emotions by analyzing the physical and social context. Review Figures 11.1 and 11.2, Animation 11.2
Speci c pattern of autonomic arousal (heart races, etc.)
Speci c pattern of autonomic arousal (heart races, etc.)
General autonomic arousal (heart races, etc.) Particular emotion experienced (fear)
Speci c pattern of autonomic arousal (heart races, etc.)
3 Facial expressions are controlled by distinct sets of facial muscles controlled by the facial and trigeminal nerves. Emotions evolved as adaptations that trigger adaptive preprogrammed sequences of behavior, and they help in social relations. Review Figures 11.8-11.10
5 Fear is mediated by circuitry involving the amygdala, which receives information both through a rapid direct route and via cortical sensory regions, allowing for both immediate responses and cognitive processing. Review Figures 11.13 and 11.14, Activity 11.1
Respiration Skin conductance Heart rate 10 20 30 40 50 60 70 80 90 100 110 120 Time (s) Attribution of emotion responsible for arousal
2 Distinct facial expressions represent anger, sadness, happiness, fear, disgust, surprise, contempt, and embarrassment, which are interpreted similarly across many cultures. Polygraphs actually measure activation of the sympathetic nervous system and therefore reflect stress, not lying. Review Figures 11.3-11.7 4 Lesions revealed an interconnected brain circuit, the limbic system (which includes the amygdala) that mediates and controls emotions. Electrical self-stimulation of some brain regions is rewarding. Review Figures 11.11 and 11.12
6 Aggression may be either proactive or reactive. Some forms of aggression are increased by androgens, such as testosterone, and seem to be inhibited by serotonergic systems in the brain. Stimulation of some limbic system regions elicits a species-typical pattern of aggression. The ventromedial hypothalamus (VMH) appears to play a central role in aggression in both sexes. Review Figure 11.16
7 Stress elevates levels of the hormones cortisol, from the adrenal cortex, and epinephrine and norepinephrine, from the adrenal medulla, while suppressing other hormones (testosterone). These responses to stress are adaptive in the short run, but in socially complex species that can experience stress for long periods, these hormonal responses decrease immune system competence, damaging our health. Review Figures 11.18-11.20, Table 11.1, Activity 11.2, Video 11.3
Percentage increased risk after controlling for other variables
70 60 40 30 0 Psychological distress at age 23
Bullied as a child Occasionally Frequently
8 The nervous, endocrine, and immune systems interact reciprocally to monitor and maintain health. Childhood stress, including being subjected to bullying, seems to increase lifelong risk for schizophrenia, depression, and suicide. Review Figures 11.21 and 11.22
The Mind's Machine digital resources include additional videos, flashcards, and other study tools.