Another hardwired fear is that of the dark (nyctophobia). Most mammals have poor night vision. There may be a predator lurking and we can't see it. This is why most horror movies have the scariest scenes in a darkened area. We are hardwired to fear open s.p.a.ces where there is no place to hide (agoraphobia), and we are hardwired to fear tight s.p.a.ces (claustrophobia), where we can't escape. Indeed, placing a rat in a tube so that it cannot move is a commonly used stress-inducing procedure in research. We are hardwired to fear loud noises (ligyrophobia), for this suggests a large animal and potential predator. We are hardwired to fear slithery (fear of snakes is called ophidiophobia) and creepy-crawly (fear of insects is called entomophobia) things. We have an emotion called disgust for hardwiring taste and smell. For mammals, there is also the fear of abandonment. This is because mammals are so helpless at birth. Without a mother there is no food or safety; there is only certain death. This is dramatically ill.u.s.trated in northern mallard ducklings, which, when separated from their mother, will follow a crude duck model, a walking person, or even a cardboard box that is moved slowly away from them. Even as an adult, fear of expulsion from your herd alters behavior, as chances for survival outside the herd are diminished. This powerful fear of abandonment has been used throughout the ages in humans as well. For example, the Catholic Church uses ex-communication and the Amish use shunning to control behavior. Fear of abandonment is one of our primal fears. For humans there are other powerful psychosocial fears that are a.s.sociated with this, including fear of loss of freedom, social standing, job, and home.

Unconditional (innate, Hardwired) Fear Stimuli Abandonment Being killed Somatic pain Heights Suffocation Novel situations Being trapped Open s.p.a.ces with no place to hide.

Ground-based predators: creepy crawly things.

Air-based predators: things out of visual field.

Nighttime and darkness.

Culture-based fears.

This hardwiring does one thing: Once the danger pattern is perceived, it produces a fear response. First and foremost, action must be taken to find a safe place, no questions asked. Evaluation of the threat follows. How do these sensory signals activate the amygdala?

Amygdala Activation.

To activate a response from the amygdala, several things must occur. First, the sensing organs need to input the unprocessed sensory information into our brain. This is a process known as transduction, the converting of one thing into another. Thus, the eye, for example, brings into the brain the visual electromagnetic spectrum. Receptors at the back of the eye transduce (convert one form of energy to another) these to electrical impulses along a neuron. After entering and being sorted by the thalamus, when appropriate, threatening stimuli (UFS) are sent to the amygdala for action. They are also sent to the visual sensory cortex where an image is formed and perceived. All sensory input is transduced to electrochemical signals that can be read and interpreted by the brain.

The thalamus acts like a complicated postal service. In addition to sending out information, the thalamus is simultaneously receiving input from other parts of the brain. The cortex sends a signal to the thalamus that increases the salience of a potential threat while diminishing the background noise. Attending to important input is a critical process and requires we minimize distractions. This is why we shut the radio off in our car if we are lost. It allows us to more easily focus on visual stimuli to aid in finding our way. If we need to be extra attentive, a physical component can be added. The external sensory organs help us focus. In the case of the eye, the macula, a dense spot of receptors, is where we focus the image when we want to pay attention. We turn our cupped ear to a sound we want to identify. We taste with the tip of our tongue. In summary, when we seek salience, we must be attentive. This allows us to spot a predator early and activate the amygdala for action. This is vigilance.

When the thalamus senses a hardwired (unconditioned) fear stimulus, it sends it directly to the amygdala for action and creates a fear response. A longer pathway, which handles the more complex aspects of the stimulus (complex content), travels from the thalamus to the cortex to the amygdala and, if appropriate, brings this refined, cortically processed sensory content to an already activated amygdala. Another pathway sends the context (background) to the amygdala via the hippocampus. Input from both sources of processed information can further excite or diminish the amygdala response. These pathways become of critical importance when we explore the mechanisms of traumatization.

If running from a predator is not a viable option, then defensive action must be taken. Fear can be converted into another survival emotion, defensive rage,13 depending on circ.u.mstances. By activating this system, we try to avoid fighting when flight is not possible.

Plan B: Defensive Rage.

Frightening a predator away avoids confrontation. Darwin describes the physiognomy of this moment as clenched jaw with the teeth exposed, snarling with an arched back, neck muscles tightened and head held straight, eyes wide and pupils dilated, nasal flaring, expanded chest, and increased height. There is an occasional roar for emphasis. This is defensive rage. This emotion and physiology occurs when fight or flight is not an option: a mother protecting her young from a powerful predator, a child being abused by a much larger adult, a person cornered by a group of thugs. While you will surely lose, the last act before engagement is to produce a moment of defensive rage, hoping to frighten your adversary. Making yourself as big and ferocious and menacing as you can be may make the predator decide not to challenge you. Defensive rage is fear mixed with anger in a situation for which there seems to be no escape (Figure 3.5).

The intruder was about to attack. Slowly she was being backed into the kitchen where she could no longer retreat. Her hands slipped over the top of the sink behind her to see if there was a weapon she could use. She found it, a sharp knife! She grasped it in her hand, arched her back, and lifted the knife blade in the air. Her mouth was clenched, her teeth were bared, and her nostrils were flaring. She stood still, waiting for the intruder to make the first move. Then she would come down on him with the blade.

Figure 3.5 Posture of defensive rage. (Courtesy of Ronald Ruden and Steve Lampasona.).

Pathway of Defensive Rage.

BLC Fear Collateral circ.u.mstances BM Defensive rage.

The expression of rage is driven by collateral circ.u.mstances at the time of the event. It is the basal medial nucleus (BM) that appears to be involved with the expression of defensive rage. Rage, like fear, has the potential to be traumatized.

In summary, the LA amygdala detects threat content directly from the thalamus or olfactory bulb in the form of sensory input and activates the amygdala. Subsequently, cortically processed sensory content also enter the LA. Contextual components of the event enter the BLA through the hippocampus (Figure 3.6). The complex content and the context provide for discrimination on whether the threat is real (e.g., is the snake on television, is it in a gla.s.s case, or if we are up Figure 3.6 Flow of information to and through the amygdala. (Courtesy of Ronald Ruden and Steve Lampasona.) close, is it really a snake or something else). As mentioned earlier, the lateral nucleus, basolateral nucleus (BLA), and the accessory basal nucleus comprise the basolateral complex (BLC).

If the threat is perceived as real, the BLC Ce output produces a preparatory physiological response that modulates the autonomic and somatic response to the stimulus. As we shall see, it is this modulation of the somatic, autonomic, and emotional components experienced during the event that is critical to explaining the consequences of a traumatization. The BLC modulates the storage and the ability to retrieve the cognitive and emotional components of the event. In certain situations the BLC can also activate the BM, amplifying defensive rage. Under suitable conditions, a flow of information can be ultimately bound together in what we call the traumatic encoding moment. How this binding process14 occurs is one of the great mysteries of the brain. Suffice it to say that it occurs.

Before we explore the process that encodes this event as a traumatic memory, a further detailed look at how emotions affect memory is given in Chapter 4.

References.

1. Wikipedia. Apparent death. Retrieved August 17, 2008, from http:// en.wikipedia.or/wiki/Apparent_Death 2. McFarland, D. (Ed.). (1982). The Oxford companion to animal behavior (pp. 180181). New York, NY: Oxford University Press.

3. Torrice, M. (2009). Pigeon wings sound the alarm. Retrieved from http:// sciencenow.sciencemag.org/cgi/content/full/2009/902/2 4. McFarland, D. (Ed). (1982). The Oxford companion to animal behavior (pp. 1314). New York, NY: Oxford University Press.

5. Whalen, J. P., & Phelps, E. A. (2009). The human amygdala. New York, NY: Guilford Press.

6. Ferreira, T. L., Shammah-Lagnado, S. J., Bueno, O. F., Moreira, K. M., Fkornari, R. V. & Oliveira, M. G. (2008). The indirect amygdala-dorsal striatum pathway mediated conditioned freezing: insights on emotional memory networks. Neuroscience 153(1): 8494.

7. Rainine, D. G., & Ressler, K. J. (2009). Physiology of the amygdala: Implications for PTSD. In P. J. Shiromani, T. M. Keane, & J. E. LeDoux (Eds.), Post-traumatic stress disorder: Basic science and clinical practice. (pp. 3978). New York, NY: Humana Press.

8. Tanimoto, S., Nakagawa, T., Yamauchi, Y., Minami, M., & Satoh, M. (2003). Differential contributions of the basolateral and central nuclei of the amygdala in the negative affective component of chemical somatic and visceral pains in the rat. Eur. J. Neurosci. 18:23432350.

9. Akmaev, I. G., Kalmillina, L. B., & Sharipova, L. A. (2004). The central nucleus of the amygdaloid body of the brain: Cytoarchitectonics, neuronal organization, connections. Neurosci. Behav. Physiol. 34:603610.

10. Akirav, I., & Maroun, M. (2007). The role of the medial prefrontal cortexamygdala circuit in stress effects on the extinction of fear. Neural Plast. 2007:30873.

11. Strange, B. A., & Dolan, R. J. (2004). Beta-adrenergic modulation of emotional memory-evoked human and amygdala and hippocampal responses. Proc. Natl. Acad. Sci. 101:1145411458.

Phelps, E. A. (2004). Human emotion and memory: Interactions of the amygdala and the hippocampal complex. Curr. Opin. Neurobiol. 14:198202.

12. Brechbuhl, J., Klaey, M., & Broillet, M.-C. (2008). Gruenberg ganglion cells mediate alarm pheromone detection. Science 321:10921095.

13. Shaikh, M. B., & Siegel, A. (1994). Neuroanatomical and neurochemical mechanisms underlying amygdaloid control of defensive rage behavior in the cat. Braz. J. Med. Biol. Res. 27:27592779.

14. MindPapers. A bibliography of the philosophy of and science of consciousness. Retrieved August 18, 2008, from http://consc.net/mindpapers/8.1e. This is a list of papers on the binding problem. Some of these papers can be viewed for free.

4.

MEMORY AND EMOTION.

To maximize the ability to avoid predation, we need the ability to encode and retrieve fear-producing memories. What are some of the processes ensuring this will occur?

Aside from fleeing and fighting, avoiding similar threatening situations in the future is important for survival. What is needed is a way to store information useful to survival, sustain its clarity, and endow it with a low threshold to recall by similar circ.u.mstances. Central to these abilities is the interaction between the amygdala and hippocampus. It is the amygdala's influence on hippocampal-directed encoding and storage of emotional memories that allows them to remain sharp and readily retrievable.

In addition to firsthand experience, we want to be able to encode useful information without necessarily having direct experience. For example, if your mother tells you that a certain place is dangerous, the thought of going there would produce a fear response, and it would probably prevent you from going. By learning without direct experience, we can safely acquire information that is useful for survival. Emotions and thoughts generated by our imagination can thus be encoded. Here, again, the amygdala and hippocampus encode emotional input arising from the mind. They a.s.sociate and store things we have heard with things we have yet to experience.

The mechanism by which a memory is stored is called consolidation. It is a process that stabilizes a memory trace after the initial acquisition. 1 Consolidation of emotional events is considered to have two distinct phases. Synaptic consolidation, which occurs rapidly, within minutes, involves glutamate receptors, norepinephrine, cortisol, and other chemicals acting in the amygdala and hippocampus. Later, system consolidation occurs as the synaptically consolidated memories become independent of the hippocampus over a period of weeks to years. These memories are stored in the cortex of the brain. (Recently, a third process has become the focus of research-reconsolidation, in which a previously consolidated memory can be made labile again through reactivation of the memory trace.) During an event that becomes traumatized, the emotional content and the a.s.sociated sensory and cognitive content become bound into an unforgettable moment. We speculate that a critical aspect of traumatization is that the unimodal sensory content remains synaptically encoded in the amygdala. Synaptic encoding of a traumatic event allows us to respond to stimuli recalling the event as if for the first time. The nonthreatening context, however, may undergo further system consolidation.

Memory Systems.

Memory storage is divided, more or less, into two separate systems. For a nonemotional event that we can describe by conscious recollection, a narrative, we are using what scientists call the declarative memory system.2 This form of memory is encoded and retrieved via the hippocampus and includes information and factual experiential knowledge. Things we can do but can't describe by narrative are stored in the nondeclarative memory, also known as procedural memory system. Procedural memory3 is the earliest memory system. It is involved with experiencing a feeling with sensory input (e.g., a perfume evokes a certain feeling), skills we learn, habits we acquire, perception of our body's posture, and conditioned responses. It helps us learn how to put food in our mouths, crawl, and speak. It is the location where emotionally intense events [e.g., abandonment or abuse] are stored before the hippocampus is operational at around the age of four. These memories are stored as a "feeling" sense; feelings that occur without cognitive content, such as a sense of safety and comfort or fear and frustration, we experience as an infant. Information stored in either memory system affects our response to subsequent events.

Jon, age 6, born in a refugee camp and adopted at age 15 months, still responded to fire engine sirens, not by covering his ears but with a comforting and defensive wrapping of his arms around his upper body and shivering. Even though he could not recall the sirens of his early childhood, he would exhibit signs of fear.

Emotion-laden events stored in procedural memory via the amygdala are part of what drives our behavior. St. Augustine suggested that while we have the appearance of free will, G.o.d predestines our lives. Freud, when he discussed his theories of psychoa.n.a.lysis, described the role of feelings stored in this manner. He interpreted St. Augustine in a different way. He felt that we do not have free will because we are driven by these subconscious memories. If these memories were traumatized, they never fade. That traumatized memories, stored below conscious awareness and not subject to ready retrieval, are of great consequence is beyond doubt.

The fundamental process required to create a memory is dependent on the neurotransmitter glutamate and its receptors. Glutamate4 is an excitatory amino acid needed for each new learning and a.s.sociating process to take place. The mechanism by which glutamate encodes these pathways remains speculative, but it involves the poteniation of post-synaptic glutamate receptors in the amygdala. A traumatic memory can be imagined as neuronal pathways connected by glutamate receptors that are laid down during the event. When reactivated by a stimulus it causes us to reexperience the original moment. This is synaptic consolidation. Interestingly, and this becomes critical in our understanding of the havening process, reactivation of synaptically consolidated glutamate pathways during recall of a traumatic memory appears to make these pathways susceptible to disruption.5 There are many neurochemicals involved with this process. One can summarize the actions of these chemicals as follows.

Neurochemicals That Facilitate Storage and Retrieval Glutamate Norepinephrine/epinephrine Acetyl choline Cortisol Dopamine Neurochemicals That inhibit Storage and Retrieval GABA.

Opioids.

Very high cortisol.

Serotonin.

The Role of Norepinephrine.

Most researchers feel that norepinephrine (NE)6 and cortisol7 are the key chemicals in the brain that enhance synaptic memory formation a.s.sociated with emotional events. As mentioned earlier, norepinephrine is released by neurons that originate in the brain stem in an area called the locus coeruleus (LC). The release of NE arises from fear stimuli that activate the Ce. The NE released enters various brain areas.

Norepinephrine enhances learning, and blocking access to its receptor inhibits learning. During an emotionally charged event, markedly increased levels of norepinephrine in the hippocampus, prefrontal cortex, and amygdala, as well as other brain areas, speak to this role. Norepinephrine appears to cause events to form stronger a.s.sociations, thus making recall easier. This critical role of norepinephrine is not limited to learning, but also plays a part in producing, from content or context, a state of altered physiology, meant to increase our chances for survival. It also plays another role in a circuit that connects the amygdala to the prefrontal cortex.

Norepinephrine in the BLC.

Research suggests that when our cortex fully evaluates a threat, and it is found not to be real, an inhibitory signal is sent from the prefrontal cortex to the amygdala. At the onset of activation of the BLC by unconditioned fear stimuli, however, the prefrontal cortex must be prevented from inhibiting amygdala outflow.8 The release of norepinephrine in the BLC appears to accomplish this. This makes sense from a survival point of view, as we don't want the thinking part of the brain to get in the way when immediate action must be taken.

The Role of Cortisol.

Cortisol has been shown to enhance synaptic memory consolidation of emotionally arousing experiences.7 It is released during stressful circ.u.mstances, and all intense emotional states activate the stress response. Cortisol potentiates norepinephrine action and is required for regulating synaptic consolidation in other brain areas.

Very high levels of cortisol released during a traumatizing event appears to affect how the event is stored in memory. These very high cortisol levels produce abnormal hippocampal activity that alters both the storage and subsequent retrieval of an intense emotional event.9 As a consequence, we cannot consciously recall the event. This is called cognitive dissociation, and the memories are only available in episodic flashbacks, intrusive thoughts, or nightmares. Where and how these memories are stored and retrieved remain uncertain. In general, the inability to consciously recall these dissociated memories is protective; we don't need to actively block the memory from our mind. Unfortunately, this consciously dissociated memory remains biologically active.

What Else Is Needed for Traumatization?

Under nontraumatizing conditions, after experiencing an emotionally charged event, the residual emotional responsiveness on recall of the memory decays over time. On the other hand, after an event is encoded as a traumatic memory, subsequent stimuli can reproduce various aspects of the event as if it were happening for the first time; there is no decrement over time. Special conditions must therefore prevail for an event to be encoded as a traumatization. Chapter 5 explores these conditions.

References.

1. Wikipedia. Memory consolidation. Retrieved June 2008 from http://en.wikipedia.org/wiki/Memory_Consolidation 2. Wikipedia. Declarative memory. Retrieved June 2008 from http:// en.wikipedia.org/wiki/Declarative_Memory 3. Tamminga, C. A. (2000). Images in neuroscience. Cognition: Procedural memory. Am. J. Psychiatry 157:162. Retrieved from http://ajp.psychiatryonline. org/cgi/reprint/157/2/162.pdf 4. Rainine, D. G., & Ressler, K. J. (2009). Physiology of the amygdala: Implications for PTSD. In P. J. Shiromani, T. M. Keane, & J. E. LeDoux (Eds.), Post-traumatic stress disorder: Basic science and clinical practice (pp. 3978). New York, NY: Humana Press.

McGaugh, J. L., Roozendal, B., & Okuda, S. (2007). Role of stress hormones and the amygdala in creating lasting memories. In N. Kato, M. Kawata, & R. K. Pitman (Eds.), PTSD: Brain mechanisms and clinical implications (pp. 89103). j.a.pan: Springer j.a.pan.

5. Nader, K., Schafe, G. E., & LeDoux, J. E. (2000). Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722726.

6. Roozendaal, B. (2007). Norepinephrine and long-term memory function. In G. A. Ordway, M. A. Schwartz, & A. Frazer (Eds.), Brain norepinephrine: Neurobiology and therapeutics. pp. 236274. Cambridge, UK: Cambridge University Press.

7. Arnsten, A. F. T. (2007). Norepinephrine and cognitive disorders. In G. A. Ordway, M. A. Schwartz, & A. Frazer (Eds.), Brain norepinephrine: Neurobiology and therapeutics. pp. 408435. Cambridge, UK: Cambridge University Press.

8. De Quervain, D. J.-F., Aerni, A., Sch.e.l.ling, G., & Roozendaal, B. (2009). Glucocorticoids and the regulation of memory in health and disease. Frontiers Neuroendorinol. 30:358370.

9. Payne, J. D., Nadel, L., Britton, W. B., & Jacobs, W. J. (2004). The biopsychology of trauma and memory. In D. Reisberg & P. Hertel (Eds.), Memory and emotion. New York, NY: Oxford University Press.