Emotions and Feelings

The Modern Search for the Emotional Brain Began in the Late 19th Century

The Amygdala Emerged as a Critical Regulatory Site in Circuits of Emotions

Studies of Avoidance Conditioning First Implicated the Amygdala in Fear Responses

Pavlovian Conditioning Is Used Extensively to Study the Contribution of the Amygdala to Learned Fear

The Amygdala Has Been Implicated in Unconditioned (Innate) Fear in Animals

The Amygdala Is Also Important for Fear in Humans

The Amygdala Is Involved in Positive Emotions in Animals and Humans

Other Brain Areas Contribute to Emotional Processing

The Neural Correlates of Feeling Are Beginning to Be Understood

An Overall View

ELATION, COMPASSION, SADNESS, FEAR, and anger are examples of emotions. These states have an enormous impact on our behavior. But what exactly is an emotion? Unfortunately, the term emotion is commonly and confusingly used in two ways. Sometimes it refers to physiological responses to certain kinds of stimuli; when in danger, your muscles tense and your heart pounds, and you may also feel afraid. But it also refers to conscious experiences, called feelings, that often (but not always) accompany these bodily responses. We need to consistently distinguish between these two states.

In this chapter we use the term emotion to refer to the first of the two states: The set of physiological responses that occur more or less unconsciously when the brain detects certain challenging situations. These automatic physiological responses occur within both the brain and the body proper. In the brain they involve changes in arousal levels and in cognitive functions such as attention, memory processing, and decision strategy. In the body proper they involve endocrine, autonomic, and musculoskeletal responses (see Chapter 47). We use the term feeling to refer to the conscious experience of these somatic and cognitive changes. In a certain sense feelings are accounts our brain creates to represent the physiological phenomena generated by the emotional state.

In sum, emotions are automatic, largely unconscious behavioral and cognitive responses triggered when the brain detects a positively or negatively charged significant stimulus. Feelings are the conscious perceptions of emotional responses.

Emotional reactions have been conserved throughout the evolution of species. Behavioral responses that we typically call emotional responses are found in very simple organisms that may not have consciousness and thus not have feelings. A bacterial cell can detect harmful and useful chemicals and respond to these in adaptive ways. Indeed, all organisms must have such capacities to survive and thrive.

Some stimuli—objects, animals, or situations—trigger emotions automatically, even in the absence of experience. These stimuli are said to have emotional competence. In addition, some otherwise insignificant objects and events that occur in conjunction with emotionally competent stimuli can acquire emotional significance through associative learning. Thus, whereas emotionally competent stimuli are naturally significant (eg, painful or delicious), other objects and events acquire emotional competence by their association with emotionally competent stimuli.

When the brain detects emotionally competent stimuli, it sends commands to networks that control the endocrine glands, the autonomic motor system, and the musculoskeletal system (Figure 48–1). The endocrine system is responsible for the secretion and regulation of hormones into the bloodstream that affect bodily tissues and the brain. The autonomic system mediates changes in the physiological control systems of the body, including the cardiovascular system and the visceral organs and tissues in the body cavity (see Chapter 47). The skeletal motor system mediates overt behaviors such as freezing, fight-or-flight, and particular facial expressions. Together these three systems control the physiological expression of emotional states.

Figure 48-1 Neural control of emotional responses to external stimuli. External stimuli processed by sensory systems converge on emotional processing systems. If the stimuli are emotionally salient, emotion systems such as the amygdala are activated. Outputs of the emotion processing systems to hypothalamic and brain stem regions activate effector cells that control the expression of physiological responses, including skeletomuscular action, autonomic nervous system activity, and hormonal release. The figure shows some responses associated with fear.

The autonomic and endocrine changes involved in emotional states are part of the body’s homeostatic regulatory mechanisms, which are engaged whenever the body is confronted by an intrinsically charged stimulus. In fact, the body’s response to strong emotion is not that different from its response to changes in other drive states or alterations in other bodily regulatory processes such as hunger, thirst, sex, and sleep, or its response to pain or changes in body metabolism that occur during vigorous exercise. These regulatory mechanisms are mediated mostly by subcortical structures—the amygdala, striatum, hypothalamus, and brain stem (see Chapter 47).

Most emotional states are observable either directly (for example, in facial expressions or other overt behaviors) or indirectly with psychophysiological or neurophysiological tests or endocrine assays. Thus many emotional responses are measurable and their neurobiological underpinnings can be investigated objectively in both human beings and experimental animals. On the other hand, measuring subjective feelings is more of a challenge and is only practical in humans.

We begin the chapter with a discussion of the historical antecedents of modern neural science research on emotion. We then describe the neural circuits and cellular mechanisms that underlie the most thoroughly studied emotion, fear. Finally, we consider how the brain processes complex social emotions and conscious feelings.

The Modern Search for the Emotional Brain Began in the Late 19th Century

The modern attempt to understand emotions began in 1890 when William James, the founder of American psychology, asked: What is the nature of fear? Do we run from the bear because we are afraid, or are we afraid because we run? James proposed that the conscious feeling of fear is a consequence of emotions, of the bodily changes that occur during the act of running away—we are afraid because we run.

According to James, each feeling (fear, joy, anger) results from its own unique pattern of emotional expression, or bodily signature, controlled by descending connections from the cerebral cortex. A feeling comes about when the bodily expression of that emotional response enters consciousness. James’s peripheral feedback theory drew on the knowledge of the brain at the time, namely, that the cortex had areas devoted to movement and sensation (Figure 48–2). Little was known about specific areas of the brain responsible for emotion and feeling.

Figure 48-2 Early theories of the emotional brain. (Adapted, with permission, from LeDoux 1996.)

William James’s peripheral feedback theory. James proposed that emotionally competent stimuli processed in sensory systems are transmitted to the motor cortex to produce emotional responses in the body. Feedback signals to the cortex convey sensory information about the body responses. The cortical processing of this sensory feedback is the “feeling,” according to James.

The Cannon-Bard central theory. Walter Cannon and Philip Bard proposed that emotions are explained by processes within the central nervous system. In their model sensory information is transmitted to the thalamus where it is then relayed to both the hypothalamus and the cerebral cortex. The hypothalamus evaluates the emotional qualities of the stimulus, and its descending connections to the brain stem and spinal cord give rise to emotional responses. The thalamocortical pathways give rise to conscious feelings.

The Papez circuit. James Papez extended the Cannon-Bard theory by adding additional anatomical specificity. The cortical region that receives hypothalamic output in the creation of feelings is the cingulate cortex. The outputs of the hypothalamus reach the cingulate via the anterior thalamus, and the outputs of the cingulate reach the hypothalamus via the hippocampus.

At the turn of the 20th century researchers found that animals were still capable of emotional responses after the total removal of the cerebral hemispheres, suggesting that some aspects of emotion are mediated by subcortical regions. The fact that electrical stimulation of the hypothalamus could elicit autonomic responses similar to those that occur as emotional responses in the intact animal suggested to Walter B. Cannon that the hypothalamus might be a key region in the control of fight-or-flight responses and other emotions.

In the 1920s Cannon showed that transection of the brain above the level of the hypothalamus (by means of a cut that separates the cortex and thalamus from the hypothalamus and lower brain areas) left an animal that was still capable of showing rage. But a transection below the hypothalamus, leaving only the brain stem and spinal cord, eliminated the coordinated reactions of natural rage. This clearly implicated the hypothalamus in emotional reactions. Cannon called these hypothalamically mediated reactions “sham rage” as they lacked input from cortical areas, which he assumed were critical for the emotional experience (Figure 48–3).

Figure 48-3 Sham rage. An animal exhibits sham rage following transection of the forebrain and the disconnection of everything above the transection (top) or transection at the level of the hypothalamus and the disconnection of everything above it (middle). Only isolated elements of rage can be elicited if the posterior hypothalamus also is disconnected (bottom).

Cannon and his student Phillip Bard proposed an influential theory of emotion centered on the hypothalamus and thalamus. According to their theory, sensory information processed in the thalamus is sent both to the hypothalamus and the cerebral cortex. The projections to the hypothalamus produce emotional responses (through connections to the brain stem and spinal cord) while the projections to the cerebral cortex produce conscious feelings (Figure 48–2). This theory implied that the hypothalamus is responsible for the brain’s evaluation of the emotional significance of external stimuli and that emotional reactions depend on this appraisal.

In 1937 James Papez extended the Cannon-Bard theory. Like Cannon and Bard, Papez proposed that sensory information from the thalamus is sent to the hypothalamus. From there, descending connections to the brain stem and spinal cord give rise to emotional responses and ascending connections to the cerebral cortex give rise to feelings. But Papez expanded the neural circuitry of feelings considerably beyond the Cannon-Bard theory by interposing a new set of structures between the hypothalamus and the cerebral cortex. He argued that signals from the hypothalamus go first to the anterior thalamus and then to the cingulate cortex, where signals from the hypothalamus and sensory cortex converge. This convergence accounts for the conscious experience of feeling. The sensory cortex then projects to both the cingulate cortex and the hippocampus, which in turn makes connections with the mammillary bodies of the hypothalamus, thus completing the loop (Figure 48–2).

In the late 1930s Henrich Klüver and Paul Bucy removed the temporal lobes of monkeys bilaterally and found a variety of psychological disturbances, including alterations in feeding habits (the monkeys put inedible objects in their mouth) and sexual behavior (they attempted to have sex with inappropriate partners, like members of other species). In addition, the monkeys had a striking lack of concern for previously feared objects (eg, humans and snakes). This remarkable set of findings came to be known as the Klüver-Bucy syndrome.

Building on the Cannon-Bard and Papez models, and the findings of Klüver and Bucy, Paul MacLean suggested in 1950 that emotion is the product of the “visceral brain.” The visceral brain included the various cortical areas that had long been referred to as the limbic lobe, so named by Paul Broca because these areas form a rim (Latin limbus) in the medial wall of the hemispheres. Later the visceral brain was renamed the limbic system. The limbic system includes the various cortical areas that make up Broca’s limbic lobe (especially medial areas of the temporal and frontal lobes) and the subcortical regions connected with these cortical areas, such as the amgydala and hypothalamus (Figure 48–4).

Figure 48-4 The limbic system consists of the limbic lobe and deep-lying structures.

A. This medial view of the brain shows the pre-frontal limbic cortex and the limbic lobe. The limbic lobe consists of primitive cortical tissue (blue) that encircles the upper brain stem as well as underlying cortical structures (hippocampus and amygdala).

B. Interconnections of the deep-lying structures included in the limbic system. The arrows indicate the predominant direction of neural activity in each tract, although these tracts are typically bidirectional. (Adapted, with permission, from Nieuwenhuys et al. 1988.)

MacLean intended his theory to be an elaboration of Papez’s ideas. Indeed, many areas of MacLean’s limbic system are parts of the Papez circuit. However, MacLean did not share Papez’s idea that the cingulate cortex was the seat of feelings. Instead he thought of the hippocampus as the part of the brain where the external world (represented in sensory regions of the lateral cortex) converged with the internal world (represented in the medial cortex and hypothalamus), allowing internal signals to give emotional weight to external stimuli and thereby giving rise to conscious feelings. For MacLean the hippocampus was involved both in the expression of emotional responses in the body and in the conscious experience of feelings.

Subsequent findings raised problems for MacLean’s limbic system theory. In 1957 it was found that damage to the hippocampus, the keystone of the limbic system, produced deficits in converting short- to long-term memory, a distinctly cognitive function. In addition, animals with damage to the hippocampus are able to express emotions, and humans with hippocampal lesions express and feel emotions normally. In general, damage to areas of the limbic system did not have the expected effects on emotional behavior.

Several of MacLean’s other ideas on emotion are nevertheless still relevant. MacLean thought that emotional responses are essential for survival and therefore involve relatively primitive circuits that have been conserved in evolution, and this notion is key to an evolutionary perspective of emotion. Further, his idea that emotional states and cognitive processes involve somewhat distinct circuits and can function relatively independent of one another, as implied by Cannon and Bard and all subsequent theories of the emotional brain, also has some merit.

The Amygdala Emerged as a Critical Regulatory Site in Circuits of Emotions

Although damage to most limbic areas does not have the effects on emotional behavior predicted by the limbic system theory, one limbic area was consistently shown to be involved in emotion. This area is the amygdala.

Studies of Avoidance Conditioning First Implicated the Amygdala in Fear Responses

In the mid-1950s Lawrence Weiskrantz sought to understand which region of the temporal lobe was responsible for the emotional changes characteristic of the Klüver-Bucy syndrome. To do this, he used avoidance conditioning, a form of instrumental conditioning.

In avoidance conditioning an animal learns to perform responses that successfully avoid an aversive shock, the unconditioned stimulus (US). Successful avoidance of shock reinforces the response, ie, it increases the probability of the response. Normal monkeys learn instrumental responses (ie, pressing a lever) to avoid the shock, but monkeys with lesions of the amygdala do not. Weiskrantz concluded that a key function of the amgydala was to connect external stimuli with their aversive (punishing) or rewarding consequences.

Fear has been a popular emotion in neuroscience research because it is so important for survival and also because excellent behavioral protocols are available for studying fear in animals. Following Weiskrantz’s discovery, many researchers used avoidance conditioning to study the neural mechanisms of fear. However fear can also be studied using Pavlovian conditioning and by the early 1980s had become the preferred protocol.

Pavlovian Conditioning Is Used Extensively to Study the Contribution of the Amygdala to Learned Fear

In Pavlovian fear conditioning an association is learned between the US (eg, shock) and the conditioned stimuli (CS) that predict the US. For example, an emotionally neutral CS (a tone) is presented for several seconds and the animal is shocked during the final second of the CS. After several pairings of tone and shock, presentation of the tone alone elicits defensive freezing and associated changes in autonomic and endocrine activity. In addition, many defensive reflexes, such as eye-blink and startle, are facilitated by the tone alone.

Pavlovian fear conditioning is actually the first phase of avoidance conditioning. The pairing of US and CS initially results in the conditioning of a response, but in the second phase the animal learns to perform an instrumental response to avoid the shock. By the early 1980s neuroscientists began to realize that a more efficient way to study fear learning is to focus on the first stage of avoidance conditioning—Pavlovian fear conditioning—and not extend the experimental design to the second phase.

Research carried out in a variety of laboratories established that lesions of the amygdala prevent Pavlovian fear conditioning from occurring. Animals with amygdala damage fail to learn the association between the CS and the US and thus do not express fear when the CS is later presented alone.

The amygdala consists of approximately 12 nuclei, but the lateral and central nuclei are especially important in fear conditioning (Figure 48–5). Damage to either nucleus, but not other regions, prevents fear conditioning. The lateral nucleus is the input nucleus receiving information about the CS (eg, a tone) from the thalamus. The central nucleus is the output region; neurons here project to brain stem areas involved in the control of defensive behaviors and associated autonomic and humoral responses (see Chapter 47). The lateral and central nuclei are connected by way of several intra-amygdala circuits, including connections in the basal and intercalated nuclei.