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References.
1. Ortony, A., Norman, D. A., & Revelle, W. (2005). Affect and proto- affect in effective functioning. In J.-M. Fellous & M. A. Arbib (Eds.), Who needs emotions: The brain meets the robot. (pp. 173202). New York, NY: Oxford University Press.
2. Tompkins, S. S. (1982). Affect theory. In P. Eckman (Ed.), Emotion in the human face (p. 355). As quoted by Kelly, A. E., Neurochemical networks encoding emotion and motivation. In J.-M. Fellous & M. A. Arbib (Eds.), Who needs emotion: The brain meets the robot (p. 34). New York, NY: Oxford University Press.
3. Nicola, S. M., Yun, I. A., Wakabayas.h.i.+, K. T., & Fields, H. L. (2004). Firing of nucleus acc.u.mbens neurons during the consummatory phase of a discriminative stimulus task depends on previous reward predictive cues. J. Neurophysiol. 91:18661882.
Wikipedia. Nucleus acc.u.mbens. Retrieved January 7, 2009, from http:// en.wikipedia.org/wiki/Nucleus_Acc.u.mbens 4. Hamann, S. B., Ely, T. D., Grafton, S. T., & Kilts, C. D. (1999). Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neurosci. 2:289293. Wikipedia. Amygdala. Retrieved January 30, 2010, from http://en.wikipedia.org/wiki/Amygdala 5. Wikipedia. Prefrontal cortex. Retrieved January 7, 2009, from http:// en.wikipedia.org/wiki/Prefrontal_cortex 6. Fellous, J.-M., & Suri, R. E. (2002). The roles of dopamine. In M. A. Arbib (Ed.), Handbook of brain theory and neural networks (2nd ed.). Cambridge, MA: MIT Press.
Ventura, R., Morrone, C., & Puglisi-Allegra, S. (2007). Prefrontal/ acc.u.mbal catecholamine system determines motivational salience attribution to both reward and aversion-related stimuli. Proc. Natl. Acad. Sci. 104:51815186.
7. DeBecker, G. (1997). The gift of fear. New York, NY: Little Brown & Company.
8. Darwin, C. (1898). The expression of the emotions in man and animals. New York, NY: Appleton and Company.
9. Wikipedia. Emotion. Retrieved May 3, 2010 from http://en.wikipedia. org/wiki/Emotion 10. Reisberg, D., & Hertel, P. (Eds.). (2004). Memory and emotion. New York, NY: Oxford University Press.
3.
ANCIENT EMOTIONS AND SURVIVAL..
Fear and rage are critical for survival because they activate our body and mind, preparing us to respond to a perceived threat. How are these emotions generated? The answer lies in an area of the brain called the amygdala.
Fear and Survival.
Tot's hair bristled: It was standing straight up. He knew he had wandered away from his mother, but the strange sounds had intrigued him. Vigilance versus curiosity. But now there was a problem because he didn't like that familiar odor. He smelled hungry predators and he was their prey. They were hyena, a mean bunch and smart, too. He knew he was in trouble. Those ancient feelings of fear had arisen to warn him, to tell him to run, but now he could not. His legs were scared stiff and he was stuck. The hyenas encircled him. His muscles tensed and as he rose up on his hind legs, he let out the best roar a young pup could. But the hyenas kept closing in. There was no escape. Tot ran in circles. The alpha male hyena was coming in for the kill, saliva already dripping from his mouth. The hyena suddenly looked up and there was Tot's mother, the largest lion cat he had ever seen. His saliva dried up, and as she leapt to protect her son, he ran, as did the others of his pack. With a roar that shook the trees, Tot's mother cuddled her son and they returned to the pride.
We all have fear hardwired in us. The open plain feels unsafe alone. Entering a dark, tight cave dries the mouth. A dark, rumbling roar sets the head in that direction.
Fear is the most ancient of emotions. It can be generated without conscious awareness. It is what makes us jump when something moves on the ground or rubs against the bottom of our leg. It makes us duck when we see something out of the corner of our eye, and it makes us run and hide, even if we are not yet aware of what the threat is. We jump, duck, run, or hide because sensory input has driven us straight into action. The patterns that motivate this response are older, much older than the human race. Much older than the thinking part of the brain. It is because of this response, however, that species have survived. Avoiding predation is something we witness, if we are aware, every day. For example, mosquitoes put their lives at stake to get blood; if they are to succeed, they must respond rapidly and correctly to avoid being squished.
Fear is personal. It makes you focus. No emotion supersedes it. It is conserved throughout all of evolution. Although we may not characterize a slug responding with avoidance to a hot flame as experiencing fear, it is the action of fear.
Fear has many moments. There is the moment of awareness. We experience a subtle, heightened sense of our surroundings, vigilance, telling us something is not right. We try to localize the fear-inducing stimulus, scanning the horizon for trouble, looking for unusual motion; scents or sounds of a potential predator become salient. If we sense something, we freeze, facing the direction of the stimulus. This freezing serves two purposes: to avoid motion so that the predator cannot see us and to allow us to focus. It is mildly activating. If we cannot discern a cause for concern, we return to what we were doing. Sometimes, however, we rationalize and shrug it off, and this can be to our peril.
At first one gazelle picked up his head from the grazing gra.s.s and scanned the horizon. What was that smell? The wind was gently flowing from the forest to the plain but nothing was moving save the gra.s.s. What was that smell? Another gazelle also picked up his head. Was it in response to the first, or was it something that he had detected? Now the focus was on the edge of the forest. Other gazelles also lifted their heads and scanned the area. Nothing? Nothing. They continued to feed and the vigilance dissipated.
Then there is the fear in the moment of danger, such as being chased by a predator. We are in full flight mode. This signal is sent from body to mind and mind to body. Our muscles become stronger, our heart beats harder and faster, our pupils dilate to see better-a struggle for survival is about to begin. We think about escape. Where can one hide? In a moment of perceived danger, the fry of the mouth-breeding cichlid fish, the Mozambique tilapia, for example, hide in their mother's mouth.
A third type of fear is a moment of panic. Overwhelmed with the feeling we are going to die, we have no direction or purpose to our actions. We are so scared we don't know which way to go to save ourselves. We literally run around in circles. All social restraints are lifted; we would kill to live. Here, too, our heart races and our muscles bulge, but we are unable to use our minds to make a plan.
Finally, there is the fear that occurs with a perceived fatal potential, a moment of imminent death. We go into another zone. Time slows down; there is no pain or other sensations. This is seen in animals after a predator has chased them. When touched, they fall to the ground and are immobile. This fear response is called thanatosis.1 Some scientists suggest this may cause the predator to relax his attention and allow the animal another chance to escape. Whether true or not, it is a state of dissociation that allows the animal to avoid the pain of being killed. Each type of fear is a.s.sociated with a unique neurobiological signature. These signatures are composed of different stress hormones flowing through the brain and body, each aiding a survival response.
Vigilance and salience are required to seek out a predator. The neurochemical dopamine is at the heart of salience. Dopamine increases the signal-to-noise ratio, making things that are salient to an immediate concern stand out against the background. Significant stimuli make their way into our conscious mind, activating centers that say, "Pay attention!" We are now in a vigilant state with another neurochemical on the rise, norepinephrine. Thus, when searching for a predatory threat, a snap of a twig may be all that is necessary to convert salience/vigilance into fight or flight. If the vigilant state was not activated, the snap of the twig may have gone unnoticed.
Flight or fight is all about two chemicals, epinephrine and norepinephrine. Epinephrine (also known as adrenaline) is peripherally secreted by adrenal glands that are located on top of our kidneys. In the same gland are cells that release another chemical critical to survival, cortisol. This is not a coincidence, and it reflects, yet again, nature's wisdom. At the same time, norepinephrine (also known as noradrenaline) is released throughout the brain from an area in the brainstem called the locus coeruleus. To prepare for a flight-or-fight encounter, epinephrine energizes the body, while norepinephrine does the same for the mind. Many changes occur during this time to improve chances of survival. One of the most dramatic is the decrease in pain sensation, a.n.a.lgesia, a.s.sociated with norepinephrine. Animals in a battle for survival do not have time to stop and lick their wounds. Boxers take multiple blows that under normal circ.u.mstances would hurt. Soldiers can sustain major injuries and continue fighting. This norepinephrine a.n.a.lgesia is critical for survival, and as we shall see, it provides an explanation of chronic pain that can be a consequence of traumatization.
Panic may occur when there is too much norepinephrine. We literally lose all ability to make rational decisions; we cannot see a way out. The planning part of the brain, the prefrontal cortex, is taken offline so all that is left is raw survival actions. The very high levels of norepinephrine shut down the executive planning branch of the brain because it will get in the way of survival. Lifeguards understand that people who are drowning will do anything, including holding them under water, to help stay afloat. No thought, just survival.
The state of dissociation, flaccidity, is about not feeling the moment. We are so terrified that sensory input slows down or ceases altogether. Nothing, or at least very little, reaches consciousness. This dissociated state is felt by some researchers to be protective. Thanatosis is about the ultimate dissociation, appearing to be dead. We can't even begin to think about movement. That is what playing dead means.
Types of Fear.
Freeze, salience, and vigilance.
Fight or flight.
Panic.
Flaccidity.
Fear Is Relayed by Our Senses.
The physiological changes produced by fear aid in survival, and fear stimuli need to be simple and readily discernable. The response to these stimuli may be present at birth or develop later. For example, the chicks of the jungle fowl2 show escape responses to loud noises, but visual escape responses to predators develop later. This makes sense because hearing a strange sound is a less complex task than recognizing a predator. In the duckling, visual patterns are recognized early. These sign stimuli can be responded to, much like noise stimuli, without prior learning (Figure 3.1). Sign stimuli (threatening content) can activate a fear response through any of the senses. For example, a silhouette when moved in one direction over a flock of ducklings induces fear. When moved in the opposite direction it does not. Why should this occur?
Figure 3.1 Visual cue stimuli can be innate. (From McFarland, D., The Oxford Companion to Animal Behavior, p. 180, Oxford University Press, New York, NY. With permission.) Flying in one direction, the short neck and long tail are characteristic of a predatory hawk, whereas flying in the other direction, the shadow looks like a goose. Since a rapid fear response is critical to survival, patterns indicating a threat must stimulate action.
Species Have Specific Alarm Systems That Activate Fear.
Animals need to avoid predation; fear helps with escape. Reactions must be based on reflex and very simple processing. Alarm responses are of two types: one that internally activates the individual for action, a fight-or-flight response, and one that serves as a warning to other members of its herd. The alarm signals that activate the herd can be visual, auditory, or olfactory. It is the source of the expression "there is safety in numbers," as many eyes are on the alert for predators. For example, pigeons, which usually feed in groups, produce an auditory alarm signal with their wings when they are startled and fly away.3 This alerts the other pigeons to a potential danger and, in an ever-expanding circle, they take off as well. Auditory alarm calls occur in many species and often have characteristics that make it difficult to locate the calling animal. These calls to other members of the species produce a "head for cover" or "cover your head" movement. Most are innate, but some are learned. An interesting example of a species-specific auditory alarm call is the yelling of "Fore!" after an errant tee shot. It makes the hearer afraid and reflexively turn away from the sound and cover his or her head.
Olfactory alarms4 activate the fear response in members of the same species. If a pike fish injures a minnow, the chemicals released from the broken skin keep other minnows away for several hours. These alarm substances most often stimulate flight but can also be used in other ways. The alarm substance of the aggressive slave raider ant not only encourages the members of the colony to fight, but also causes panic in workers of other ant species, making them more vulnerable to attack.
Fear Activates Physiological Changes.
A fear response produces a change in our physiology. Our body is put on alert. Increased muscle strength, increased oxygen availability, Figure 3.2 Anatomy of the brain. (Medical ill.u.s.tration provided courtesy of Alzheimer's Disease Research, a program of the American Health a.s.sistance Foundation, 20002010, http://www.ahaf.org/alzheimers/) increased sensory acuity, and the halting of nonsurvival processes such as digestion and grooming are all necessary so we focus only on action. Our mind is put on alert, to try to seek an escape and prepare us to store vital information so that this circ.u.mstance can be avoided in the future. From an evolutionary point of view it makes sense that there be one coordinating center. It is called the amygdala. Operational at birth (maybe even before), it undergoes changes as the individual matures.5 The amygdalae are almond-shaped groups of neurons, located on both sides of the brain. Each has its own function. The right amygdala, considered the one in command during fear situations, is located just off the midline, deep inside the temporal lobe. Its location is ideally suited to receive and send information to other areas of the brain (Figure 3.2). It is part of our primitive survival apparatus called the limbic system.
The Limbic System.
The limbic system is a construct, loosely defined anatomically, but with a specific function. It is preserved through all mammalian evolution. Its role is to coordinate the activity of various parts of the brain that relate to improving our chances of survival. Some of the anatomical structures a.s.signed to the limbic system include: Amygdala-involved with emotional expression (fear/rage), memory, and learning.
Hippocampus/Fornix-Involved with learning and storage and retrieval of an event. The fornix connects the hippocampus to the thalamus and hypothalamus.
Thalamus-Receives and sends sensory information and it is modulated by other brain centers.
Cingulate gyrus-Related to orienting to a threatening stimulus and attention.
Hypothalamus-Involved with the release of stress hormones. Prefrontal cortex-Generally considered an inhibitor of responses arising from the limbic system. Among its functions is threat evaluation.
While the limbic system has many roles, for the purposes of this book it is the ability of this system to encode information vital to survival that is critical. In most mammals, survival is equivalent to escape from a predator. The individual learns not to go where danger lies. In humans, we can survive yet not escape the moment. For example, in a car crash where we are inescapably trapped in the moment. These circ.u.mstances produce extreme emotions without a perceived escape. As a consequence and described in detail later, the limbic system inappropriately traumatizes these moments, such that stimuli that recall the moment can reproduce both the emotional and physical experience at the time of the event. In the adult, a functioning limbic system is necessary for traumatization.
In early life, when the limbic system has not completely formed (the hippocampus is not yet functional), highly emotional moments that occur become stored in a separate memory system called procedural memory (see p. 38). This memory system is felt to be located in the dorsal striatum. Although not formally part of the limbic system, it encodes the components of powerful early emotional states via the amygdala5. While the cognitive (narrative) component of the event itself is not stored, it affects us nonetheless.
Input Into the Amygdala From Senses.
The thalamus receives input from four senses: sight, taste, touch, and hearing (Figure 3.3). Smell, our most primitive sense, has olfactory neurons that bypa.s.s the thalamus and head directly to the cortex and, if appropriate, the amygdala. This allows for very rapid, out-of-sight distance evaluation. It is not a good thing to be upwind of a predator. In addition, the thalamus sends its input to the cortex for further processing and, if appropriate, send this processed information to the amygdala.
The right amygdala is a remarkable coordinator for emotional and physiological responses and is made up of a number of areas, called nuclei, each having different functions (Figure 3.4).
Perceived unimodal threatening content (e.g., a loud sound) is directly relayed from the thalamus to the lateral amygdala (LA) as a UFS, signaling danger.
Threatening unimodal content/UFSThalamusLA In addition to entering the LA, the unimodal content also combines with other aspects of the threatening content such as movement, odor, size, shape, and visceral sensation to produce complex content that travels from the thalamus to the cortex also entering the LA.
Complex contentThalamusCortexLA The sensory stimuli that remain outside the complex content is called the context. This travels from the thalamus to the cortex and enters the basolateral amygdala (BLA) via the hippocampus.
Figure 3.3 Pathways from sensory organs to brain areas.
Figure 3.4 Diagram of the amygdala. LA, lateral nucleus; BLA, basolateral nucleus; BM, basomedial nucleus; Ce, central nucleus; AB, accessory basal nucleus. (Courtesy of Ronald Ruden and Steve Lampasona.) Sensory ContextThalamusCortexHippocampusBLA The accessory basal nucleus (AB) is where threatening olfactory content directly enters the amygdala.
Threatening olfactory stimuliAB While each area of the amygdala has separate functions, there is much overlap and the neuroanatomy is very similar. For simplicity, these three nuclei, the LA, BLA, and AB, comprise what is called the basolateral complex (BLC).7 The BLC is where threatening content begin the process of activating action and emotion.
LA/BLA/AB = BLC.
Outflow From the Amygdala.
The emotional response to a threat is dependent on the BLC activating another part of the amygdala, the central nucleus (CE). The Ce activates and coordinates coordinates the physiological response8 to sensory input that modulates somatic, endocrine, and autonomic processes. The Ce sends signals to the areas that are involved in fight or flight, danger evaluation, motivation to action, salience and vigilance, orienting, freezing, memory, and pain perception (Table 3.1).9 Table 3.1 Outflow From the Central Nucleus Emotional Stimuli Thalamus BLC Ce Psychological Responses BRAIN AREA.
RESPONSE.
Sympathetic activation Prepare us for flight or fight Prefrontal cortex Aid in danger evaluation Nucleus acc.u.mbens Motivate us to action Ventral tegmentum Increase salience Locus coeruleus Increase vigilance Central grey Cause freezing.
Insula and amygdala.
Mediate pain perception.
The medial prefrontal cortex (mPFC) as the evaluator of danger is particularly critical for traumatization and has a reciprocal relations.h.i.+p with the amygdala. When the BLC amygdala first perceives fear it inhibits the mPFC, preventing it from shutting down the fear response. This allows the body and mind to prepare for flight or fighting. Under circ.u.mstances where evaluation of the threat is made and found not to be significant, the mPFC then sends an inhibitory signal to the amygdala and suppresses the response. Under extreme fear, anger, or chronically stressful conditions this inhibitory signal sent by the mPFC may be reduced and unable to modulate the outflow from the amygdala. This observation suggests a mechanism for kindling, a process that predisposes to future traumatization.10 The BLC also sends information to the hippocampus,11 a critical structure for encoding and retrieval of the cognitive component. Finally, the BLC is the site where the sensory components of the content (unimodal and complex) and context begin the process leading to their a.s.sociation.
Hardwired Fears: Unconditioned Fear Stimuli (UFS) Directly Enter the Amygdala.
What makes input appropriate to be sent to the amygdala? Stimuli that activate the amygdala without prior learning are sensory content called unconditioned fear stimuli (UFS) and are considered innate. These stimuli are recognized and sent directly to the amygdala; no thought is required. Recently, researchers have uncovered a hardwired pathway that produces a fear response.12 In an experiment, mice placed in a box are stressed and exhibit signs of fear. When this occurs the researchers transfer the air in this box to another box where another mouse is quietly waiting. In the nose of the mouse is a cell called the Gruenberg ganglion that goes directly from the nose to the olfactory alarm system. This cell recognizes alarm odors secreted by frightened mice. In short order, the quiet mouse begins to exhibit signs of fear. In a second set of experiments the researchers cut the connection between the ganglion and the olfactory system in the nonstressed mouse, metaphorically cutting the electrical connection in the mouse's nose. Using conditions identical to the first experiment, the quiet, unstressed mouse fails to respond to the air from the box of the stressed mouse. The conclusions from this study are that mice give off an odor (unimodal sensory content) to warn other mice, but when the neuron containing the receptor for this alarm odor is severed, the warning is not received. This is an example of how nature literally hardwires responses to fear stimuli.
Avoiding Threats to Survival.
To avoid predation, action is required. Thought and planning are too slow under most circ.u.mstances. Try to catch a fly on the wing and witness astonis.h.i.+ng avoidance behavior without thought. In most species, including humans, the brain sends unconditioned (innate, hardwired) fear stimuli directly to the amygdala, alerting us to get out of there. These circuits generate action. No evaluation is necessary. The goal is to avoid the potential predator. We find that a rapidly dropping horizon, or what we call fear of heights (acrophobia), is one of them. Try standing on a rooftop next to the edge. A dropping horizon is one in which we don't know where our leading foot will land or, if we do know, it's not good. A dropping horizon produces fear without a.s.sessment. This innate fear of dropping horizon becomes important in understanding certain phobias, such as fear of heights, bridges, ladders, and so on.