13: Emotions Cognitive Neuroscience David Eagleman Jonathan Downar

Chapter Outline Early Theories of Emotion Core Limbic Structures: Amygdala and Hypothalamus The Limbic Cortex and Emotions Limbic Association Cortex: Modulation of Emotion Neurochemical Influences on Emotion

Early Theories of Emotion Emotional Expressions: Signposts on a Landscape of Inner States The James-Lange Theory of Emotion: A Bottom-Up Theory The Cannon-Bard Theory: A Top-Down Theory Two-Factor Theories: Reconciling Central and Peripheral Influences on Emotion

Emotional Expressions Emotions allow us to signal our internal state to others. Animals have similar emotions to humans. The study of human emotions goes back to Darwin, who suggested that emotions are constant across cultures and ages. Emotions include fear, anger, surprise, joy, sadness, and disgust.

Emotional Expressions FIGURE 13.3 Basic emotions, such as (a) fear, (b) anger, (c) surprise, (d) joy, (e) sadness, and (F) disgust, can be identified across cultures.

The James-Lange Theory of Emotion According to this theory, the physiological reaction in the body causes the emotion. Fight or flight system reacts very rapidly to stimuli. This is a bottom-up theory because stimuli are detected by the peripheral nervous system and transmitted to the brain.

The James-Lange Theory of Emotion FIGURE 13.4 The James–Lange (bottom-up) and Cannon–Bard (top-down) theories of emotion. (a) In the James–Lange theory, physiological signals travel up from the visceral organs of the body to produce emotional states in the brain. (b) In the Cannon–Bard theory, emotional states arise in the brain, which then sends signals down to produce physiological reactions in the visceral organs of the body.

The Cannon-Bard Theory This arose as a criticism of the James-Lange theory. Many bodily responses are too slow to generate an emotional response. Artificially triggering sensations in the body does not induce emotions. This is a top-down theory, because information about the emotion spreads from the brain to the body.

The Cannon-Bard Theory This theory proposes that the thalamus relays sensory information to the cortex and to the hypothalamus. The cortical pathway results in the perception of the emotion. The hypothalamic pathway coordinates the emotional response within the body.

Two-Factor Theories Emotions do not need to be either top-down or bottom-up. Emotions could involve some combination of both theories. The two-factor theory was developed to address this.

Two-Factor Theories Schacter and Singer’s experiment: Subjects were injected with either saline or epinephrine to manipulate the physiology. Of those injected with epinephrine, half were told of the effects and half were not to affect the cognitive context. Subjects interacted with an actor. Both physiology and cognition affected the subject’s emotional state.

Two-Factor Theories FIGURE 13.7 The Schachter–Singer theory of emotion. (a) According to this two-factor theory, both the visceral response to the stimulus and the cognitive evaluation of this stimulus contribute to the emotional response. (b) Summary of Schachter and Singer’s 1962 experiment. Subjects’ emotional responses to an injection of epinephrine depended on whether they interacted with an angry or euphoric person. If they were told ahead of time about the bodily effects of the injection, the emotional response was weaker.

Two-Factor Theories FIGURE 13.9 Summary of the three theories of emotion. (a) The James–Lange theory, a bottom-up theory; (b) the Cannon–Bard theory, a top-down theory; and (c) the Schachter–Singer theory, a two-factor theory.

Core Limbic Structures: Amygdala and Hypothalamus Hypothalamus: Internal States, Homeostatic Drives Do Hypothalamic Circuits Generate Inner Emotional Experiences? Amygdala: Externally Generated States and Drives The Amygdala and Emotional Experience Hippocampus: Emotional Memories

Core Limbic Structures: Amygdala and Hypothalamus Ventral Striatum: Pleasure and Reward Bringing It All Together: The Circuit of Papez and the Ring of Limbic Cortex

Hypothalamus: Internal States, Homeostatic Drives The hypothalamus and the amygdala are important limbic structures. The hypothalamus contains many different nuclei, which influence reproductive, appetitive, and agonistic behaviors. Receptors in the bloodstream monitor the composition of the blood and report that to the hypothalamus.

Hypothalamus: Internal States, Homeostatic Drives FIGURE 13.10 The hypothalamus and survival drives. The nuclei of the hypothalamus coordinate core survival functions, including homeostatic drives, agonistic drives, and reproductive drives.

Hypothalamus: Internal States, Homeostatic Drives FIGURE 13.11 Major input pathways to the hypothalamus. Inputs come from the visceral sensory neurons of the spinal cord, visceral sensory nuclei within the brainstem, limbic regions of the cortex, and from the hippocampus and amygdala.

Hypothalamus: Internal States, Homeostatic Drives FIGURE 13.12 Regions of the brain where the blood–brain barrier is more permeable. These regions act as “windows” through which the hypothalamus and other brain regions can sense the chemical and hormonal composition of the blood, to monitor the internal environment.

Hypothalamus: Internal States, Homeostatic Drives The hypothalamus can affect the internal state via three pathways. The autonomic output pathway stimulates the sympathetic and parasympathetic nervous systems. The neuroendocrine pathway regulates hormone levels throughout the body. The motivational pathway stimulates the forebrain to generate complex plans.

Hypothalamus: Internal States, Homeostatic Drives FIGURE 13.13 Three output pathways from the hypothalamus. An autonomic pathway regulates the sympathetic and parasympathetic nervous system; a neuroendocrine pathway regulates hormone secretion in the pituitary gland; a motivational pathway up through to the cerebral cortex sets behavioral priorities.

Hypothalamic Circuits Generate Inner Emotional Experiences The hypothalamus is the first level of the nervous system that brings together Survival-relevant stimuli Internal drives caused by these stimuli A means to change the internal state to respond to the stimuli

Amygdala: Externally Generated States and Drives Much of the input to the amygdala is from the outside world. Output from the amygdala Down to the brainstem and spinal cord To hypothalamic nuclei that are important for secreting hormones Up to the striatum and the cortex

Amygdala: Externally Generated States and Drives FIGURE 13.15 The amygdala. (a) Input pathways to the amygdala. (b) Some of the major subdivisions of the amygdala, including the basolateral nuclei and the centromedial and cortical nuclei.

Amygdala: Externally Generated States and Drives The basolateral amygdala tracks value and projects to the cortex. The centromedial amygdala projects to and influences the hypothalamus and brainstem. The amygdala is important for fear learning in classical conditioning experiments.

Amygdala: Externally Generated States and Drives FIGURE 13.16 The classical conditioning pathways in the amygdala. An unconditioned stimulus (US), pain, and a conditioned stimulus (CS), a noise, are presented together. Both the US and the CS stimulate the basolateral amygdala and are paired together, stimulating the central nucleus of the amygdala. The output from the central nucleus triggers the freezing behaviors and activation of the autonomic nervous system. Over a few trials of learning, the connections between these nuclei are strengthened, so that the noise comes to trigger the response on its own.

The Amygdala and Emotional Experience Damage to the amygdala can impact behavior and emotions. Monkeys with bilateral damage to the amygdala develop Kluver-Bucy syndrome. In humans with damage to the bilateral amygdala, patients have difficulty learning and expressing fear.

Hippocampus: Emotional Memories The hippocampus can be functionally subdivided into the posterior and anterior hippocampus. The posterior hippocampus is involved in spatial functions. The anterior hippocampus is involved in emotional memory.

Hippocampus: Emotional Memories FIGURE 13.18 The location of the hippocampus within the temporal lobe.

Hippocampus: Emotional Memories FIGURE 13.19 The amygdala and hippocampus and their contributions to memory. The amygdala and anterior hippocampus are important for emotional episodic memories, and the posterior hippocampus is important for spatial memories and navigation.

Ventral Striatum: Pleasure and Reward Electrical stimulation of the septal area, near the ventral striatum, provides intense reward. Rats will push a lever to receive stimulation here to exclusion of all other activities. This region shows increased activity during many rewarded behaviors.

Ventral Striatum: Pleasure and Reward FIGURE 13.20 Electrodes implanted into the septal area of a rat, near the medial forebrain bundle. The rat repeatedly presses a lever to receive stimulation, as if the stimulation itself is rewarding. This region became popularized as a “pleasure center” within the brain.

Ventral Striatum: Pleasure and Reward FIGURE 13.21 Effects of deep brain stimulation (DBS) in the ventral striatum. In patients with treatment-resistant depression, DBS of the nucleus accumbens results in decreased activation in frontal regions of the brain and decreased symptoms of depression for some patients.

The Circuit of Papez and the Ring of Limbic Cortex Interconnected areas involved in emotional responses. Hypothalamus monitors the internal environment. Amygdala monitors the external environment. Anterior hippocampus generates emotional states based on past experiences. Ventral striatum represents reward value.

The Circuit of Papez and the Ring of Limbic Cortex FIGURE 13.22 Circuit of Papez. These interconnected brain areas are important for controlling emotional expression and were first described by Papez in 1937. The areas involved include the thalamus, hippocampus, amygdala, and hypothalamus/mammillary bodies. The arrows represent the flow of information through the circuit.

The Limbic Cortex and Emotions The Interoceptive Insula: The “Feeling” Side of Emotions Cingulate Cortex: A Motor Cortex for the Limbic System Ventromedial Prefontal Cortex: A Generator of Gut Feelings

The Interoceptive Insula: The “Feeling” Side of Emotions The limbic regions are important for generating and modulating emotional states. The insula regulates the sensory, subjective experience of emotions. The insula produces whole-body sensations that are associated with emotional states.

The Interoceptive Insula: The “Feeling” Side of Emotions FIGURE 13.23 The core region of the limbic sensory cortex is the insula. (a) The insula represents the body’s internal state. (b) Internal sensory neurons (interoceptors) from the visceral organs send signals through the spinal cord and brainstem to the ventromedial nucleus of the thalamus, which serves the posterior insula.

The Interoceptive Insula: The “Feeling” Side of Emotions FIGURE 13.24 Distinct roles of the anterior and posterior insula. The posterior insula represents basic visceral sensations like pain, temperature, fatigue, or itch. The anterior insula represents the more complex whole-body sensations associated with emotional states: feelings of sadness, happiness, anger, disgust, or elation.

Cingulate Cortex: A Motor Cortex for the Limbic System The cingulate cortex provides motor control for the autonomic nervous system, brainstem, amygdala, and hippocampus. The cingulate gyrus contains many sub-regions, each of which influences different targets.

Ventromedial Prefontal Cortex: A Generator of Gut Feelings Iowa Gambling Task Subjects pick cards from a risky deck of cards, with large gains and larger losses, for a safe deck, with smaller gains and losses. Over time, subjects learn that picking from the safe deck gives them more money.

Ventromedial Prefontal Cortex: A Generator of Gut Feelings FIGURE 13.26 The Iowa gambling task. Players can pick from the risky deck, where the gains are greater, but so are the losses; or they can pick from the safer deck, where the gains are smaller, but so are the losses.

Ventromedial Prefontal Cortex: A Generator of Gut Feelings Patients with damage to the ventromedial prefrontal cortex cannot get along well in daily life, despite normal intelligence. This structure uses somatic markers, gut feelings that suggest danger, to influence behaviors. Patients with damage to this area do not switch their behavior on the gambling task.

Ventromedial Prefontal Cortex: A Generator of Gut Feelings FIGURE 13.27 Brain activation for decision making using external versus internal cues. (a) Subjects who have to report the suit of a nonhidden card can use external cues: the visual appearance of the card. The dorsolateral prefrontal cortex, which guides behavior using external cues, is active during this “card-reporting task.” (b) Subjects who have to guess the suit of a hidden card can only use “gut feelings,” or internal cues. The ventromedial prefrontal cortex is active for card-guessing rather than card-reporting.

Ventromedial Prefontal Cortex: A Generator of Gut Feelings The ventromedial prefrontal cortex affects activity in the hypothalamus, anterior hippocampus, and brainstem. Through these connections, the ventromedial prefrontal cortex learns and generates visceral responses to stimuli.

Ventromedial Prefontal Cortex: A Generator of Gut Feelings FIGURE 13.28 Activity in the dorsolateral prefrontal cortex (VMPFC) and other brain areas decreases as the perceived reward value decreases. When subjects were overfed chocolate, they went from liking it to disliking it. At the same time as their subjective rating of the desirability of chocolate decreased, activity in the VMPFC also decreased.

Limbic Association Cortex: Modulation of Emotion The Mechanisms of Emotional Reappraisal Brain Injury, Brain Stimulation, and Emotion Regulation

The Mechanisms of Emotional Reappraisal The adjustment of emotional response based on context is known as reappraisal. There are changes in the activity of the lateral prefrontal cortex and anterior insula when a subject reappraises the situation. There are also changes in connectivity between different regions during reappraisal.

The Mechanisms of Emotional Reappraisal FIGURE 13.31 Mechanisms of successful cognitive reappraisal. A set of areas in the prefrontal cortex are active during successful regulation of emotional responses. They exert their effects by influencing the response of the nucleus accumbens and amygdala to an emotional stimulus. When they succeed in altering the activity of these structures, cognitive reappraisal is successful.

The Mechanisms of Emotional Reappraisal In healthy subjects, the ventrolateral prefrontal cortex activates the ventromedial prefrontal cortex. This reduces autonomic and amygdala responses to the stimulus. In depressed patients, the ventromedial prefrontal cortex increases autonomic and amygdala responses to the stimuli.

The Mechanisms of Emotional Reappraisal FIGURE 13.30 The ventromedial and ventrolateral prefrontal cortex can decrease amygdala activity during emotion-regulation. But in depressed patients, the opposite effect occurs.

Brain Injury, Brain Stimulation, and Emotion Regulation Brain injuries to the regions other than the prefrontal cortex seem to decrease the incidence of depression. Dorsomedial prefrontal cortex injuries increased the incidence of depression. Activity in other prefrontal areas has been shown to impact mood disorders in other studies.

Brain Injury, Brain Stimulation, and Emotion Regulation FIGURE 13.32 Effects of brain lesions on depression severity in combat veterans. Veterans with lesions in DMPFC have a high incidence of severe depression compared to veterans with no lesions or those with lesions outside the frontal lobes. Lesions to VMPFC have the opposite effect and actually appear protective against severe depression.

Brain Injury, Brain Stimulation, and Emotion Regulation FIGURE 13.33 Effects of left and right DLPFC brain lesions on depression incidence in combat veterans. Neither left nor right DLPFC lesions cause a higher risk of depression in veterans. The incidence of depression is actually slightly lower in these groups compared to veterans without lesions.

Neurochemical Influences on Emotion Serotonin and Mood Norepinephrine and Mood GABA and Anxiety

Serotonin and Mood Serotonin plays an important role in regulating mood. Subjects on a diet low in tryptophan, a precursor to serotonin, have a negative mood bias. Subjects also change connectivity in the ventral striatum and ventromedial prefrontal cortex to resemble patients with depression.

Serotonin and Mood FIGURE 13.35 The serotonin pathways in the brain. Note that serotonin-containing neurons project to many different areas of the cortex, brainstem, and spinal cord, and thus perform a wide variety of functions. The mood-altering effects of serotonin are just one of these many functions.

Serotonin and Mood Selective serotonin reuptake inhibitors (SSRIs) alter mood. These are commonly used to treat depression. Even low doses can remove the negative mood bias. Use of SSRIs improves confidence and cooperative behaviors.

Serotonin and Mood FIGURE 13.36 Effects of serotonin on the amygdala response to emotional faces. A single dose of a selective serotonin reuptake inhibitor (SSRI) can abolish the amygdala’s response to faces with fearful emotional expressions.

Norepinephrine and Mood Some antidepressant medications affect norepinephrine by blocking its reuptake into the presynaptic cell. Effects of increasing norepinephrine are similar to increasing serotonin.

Norepinephrine and Mood FIGURE 13.37 The norepinephrine pathways in the brain.

GABA and Anxiety GABA is the most common inhibitory neurotransmitter in the brain. Benzodiazepines increase the effect of GABA, thereby decreasing activity in the brain. These can be used to decrease excitability, and therefore anxiety.

GABA and Anxiety FIGURE 13.38 Effects of benzodiazepine medication on brain activity during anticipatory anxiety. (a) During scanning, subjects saw a light predicting the delivery of a painful hot stimulus to the hand. Their anticipatory anxiety was then treated with either placebo or a benzodiazepine. (b) The anterior cingulate and anterior insula were activated during anticipatory anxiety, before the painful stimulus was delivered. however, if given a benzodiazepine, this activity was reduced, and anxiety diminished.

GABA and Anxiety FIGURE 13.39 GABA receptor distribution in the mouse brain. (a) The mid-sagittal anatomy of the mouse brain, showing major brain regions and structures. (b) Regions where the alpha-2 GABAA and alpha-3 GABAA receptors are found. Note the high concentration of alpha-2 receptors in limbic areas: hippocampus, hypothalamus, basal forebrain, and ventral striatum. Benzodiazepine medications act via this receptor subtype to inhibit activity in these areas, which reduces anxiety.