The Best Defense
I don’t even call it violence when it’s in self defense; I call it intelligence.
Malcolm X, speech to Peace Corps Workers, December 12, 1964
Until recently, the accepted view was that there is a single brain circuit that underlies all types of fear and aggression. We now see that this view was the consequence of analytical tools that were too blunt to resolve the intricate details. New research on lab rats and mice has identified distinct circuits for fear and aggression in response to pain, predators, attack from members of the same species, and in mothers protecting their young. Different provocations trigger different threat-detection circuits in the brain that activate different response circuits to drive various behaviors of aggression or submission.
Momma Bear
Former Alaskan governor and US vice presidential candidate in the 2010 election, Sarah Palin, referred to herself during the campaign as a “momma grizzly.” What she instantly conveyed in this comment was the well-appreciated and powerful biological imperative about the so-called weaker sex. Females are not normally physically aggressive like their notoriously warmongering, brutish, and brawling male counterparts, but females are capable of snapping in vicious violence when necessary—especially to protect their young. Sarah Palin is an avid outdoors enthusiast and hunter, so she likely knew this animal behavior firsthand, but all women (and men) resonated with the biological truth: Don’t ever get between a mother and her child.
A mother moose and her calf had wandered onto campus at the University of Alaska, Anchorage, and the two were quickly adopted as the unofficial campus pets. They were cute. Comical-looking animals with big black eyes, large furry ears, and a goatee-like beard, moose evoke the Bullwinkle cartoons of simple-minded, friendly creatures. The females, who lack the regal antlers of males, are especially amusing beasts.
Moose are enormous, though. The largest species in the deer family, moose stand more than six feet high at the shoulder when mature. Males weigh up to 1,500 pounds, females typically half that. Moose are peaceful animals. Being herbivores, they have no reason to attack other animals to feed and they are not aggressive toward humans. Despite this, more people are injured by moose than by bears and wolves combined.
As with most grazing animals, moose are preyed upon by carnivores, but moose are far from defenseless. Protected not only by their bulk, moose, unlike other members of the deer family, can kick in all directions, including sideways. Unlike with, say, a horse, there is no safe direction from which to approach a moose. Moose have very flexible joints and sharp, pointed hooves, and the 1,500-pound beasts kick powerfully with both their front and back legs.
As seen captured on video a seventy-one-year-old man, Myong Chin Ra, is walking carefully on a slick, snow-covered sidewalk bordered by three feet of shoveled snow, ambling in his gray wool cap toward the entrance of the Campus Sports Center at UA Anchorage, to meet his wife for lunch. The moose and her calf are not far from the glass doors leading into the facility. The calf is standing in the corner of the entryway and its mother stands behind. Both of them are facing the corner. The animals are off to the side of the vestibule; neither one blocks the entrance.
Suddenly, the mother moose turns and looks back at the elderly man over her left shoulder. The man briskly diverts his course to scamper away, but his escape is slow on the icy path. Suddenly the moose charges explosively in three body-length bounds at full speed toward the fleeing man. She rises up on her hind legs and crashes down on the man’s shoulders from behind with her two forelegs, bringing her full weight crushing down on him as he attempts to escape. Mr. Ra crumples facedown onto the ground. The momentum of the tackle propels the moose over the victim’s prostrate body but she delivers a powerful kick to the man’s back with her right hind leg as she tramples over him. She pivots instantly; swinging back toward the fallen man she begins stomping him with all four legs, dancing over the helpless victim and delivering rapid, powerful blows like a flurry of invisible punches from a prizefighter, but each blow delivers the force of a jackhammer. The moose continues the vicious attack, circling again and coming back to finish him off with a blaze of vicious kicks. The curious baby moose comes over to watch the fray. The mortally wounded man lay on his right side in the fetal position trying to protect himself from further attack, but the animal kicks and stomps him about the head and upper body.
Myong Chin Ra was rushed to the hospital, but he died from the large number of severe blows he received within a period of less than three seconds.
Mike MacDonald, a game expert, explains that the moose was acting instinctively to protect her young. Even though the elderly man made no threatening actions at all, the situation from the perspective of the moose appeared to place her calf in potential danger.
“She had the building behind her and snow berms on either side of her, so she was pinned in.”
Although the man had not provoked the animals in any way, witnesses later stated that students had teased the pair hours earlier. “There were people standing around throwing snowballs, yelling, whistling, shouting, trying to get their attention,” said Ann Gross, a director at the university’s day-care center next to the sports center.
Appreciating that this was a natural, instinctive defensive behavior, university authorities decided not to kill or capture the moose because of this freak incident. Instead, they posted signs on campus educating the college community about the need to keep a safe distance from the animals.
Five days later, the same moose attacked psychology professor Bruno Kappes in a very similar chance and unprovoked encounter.
“I think my response was a normal panic response,” he told Anchorage Daily News reporter Sheila Toomey a few days afterward, with obvious gashes on his battered forehead.
“Fortunately I had seen the power and viciousness of this animal, and that was significant in appreciating what the animal could do to me.
“I knew when the ears went down and it stretched its head out at me, I knew it was preparing to launch toward me . . . otherwise I probably would have just said ‘Nice moose,’ and tried to walk around it.” Instead, Kappes instantly darted away as fast as he possibly could.
Kappes was saved by the hardwired defensive threat-response circuits in his brain. Instantly he felt his body’s own powerful fight-or-flight response engage, and that explosive neurophysiology saved his life.
The adrenaline rush kicked in just as it was supposed to, he said to the reporter afterward. “That’s why I was able to jump probably 10 feet in the air. They said I also changed direction in midair.”
“It was like the professor was just shot out of a cannon,” campus police officer Richard Altman said, as he rushed toward the scene and drew his gun. “Back up! Get behind me!” Altman commanded. Kappes responded as ordered.
The psychologist, who, ironically, is an expert on PTSD, suddenly found the tables turned. “Let’s say this: I look for moose in my house.”
For the safety of people on campus, the decision was made to kill the moose.
This episode with the mother moose illustrates the Family trigger of rage. It is a primordial, instantaneous trigger of violence shared by many animals, large and small, weak and strong, predators and prey. The young are the weak point in the cycle of life, and nearly all animals have been programmed through evolution to immediately sacrifice all to save their offspring from danger. This is the core of what it is to be a parent.
The magnitude of the danger can be immaterial to a mother who suddenly finds her child in jeopardy. Her response is immediate. Security cameras in the London Underground system captured an example of this on July 23, 2014. A whoosh of strong wind produced by a subway train blows against a blue stroller carrying a baby as the mother is distracted tending to her luggage. The stroller rolls slowly off the platform and falls onto the steel tracks. Instantly the young mother leaps onto the tracks, snatches her baby, stroller and all, and hoists her child back onto the platform to safety. Then she springs back up onto the chest-high platform with the sudden strength of a gymnast as the rails begin to glow with the reflection of headlights from the oncoming train. She escapes seconds before the train barrels into the station. Her male companion drops to his knees to embrace the stroller. It could have been a scene from a superhero movie, except that the petite blonde with her hair piled up on her head and wearing a “girly” backpack stuffed with baby supplies, looks seriously miscast.
Threat-Response Neurocircuitry
The circuitry for the Family trigger is tripped when a mother rat snaps violently to protect her young and attacks a male intruder. Laboratory research shows that this response involves three brain areas: amygdala (sentry for danger); hypothalamus (hormonal and autonomic regulation); and septum (triggering bodily responses). There are discrete circuits in each of these brain regions that operate in controlling maternal aggression. For example, olfactory cues from a male intruder that communicate to the MEA region of the amygdala are critical in triggering maternal aggression in rodents.
Other brain regions are also involved. The cerebral hemispheres contain a hollow, fluid-filled space called the lateral ventricle. An arc of brain tissue surrounding the lateral ventricle forms the limbic system. This brain region functions to help an individual cope with their environment and especially cope with other members of the same species in the environment. In short, the limbic system is the brain’s sentry for danger, as was discussed previously in the chapter on fear. Naturally this system needs widespread connections throughout the brain to carry out this complex function of threat detection and rapid response. Many of these functions influenced by the limbic system are automated behaviors related to food, sex, and threats of various types, which are conveyed to us as feelings or emotions—fear, hunger, anger, and so on. There are interactions between the amygdala and the hippocampus to coordinate time and space with experiences, past and present, in the present threat environment. These activities recording context and experience make the hippocampus critical for forming and recalling many kinds of memory, and this connection between fear and memory is the substrate for PTSD.
The amygdala, a central part of this system, serves to monitor complex status information about the body and changing environmental factors and then grab the attention of the cerebral cortex to make us consciously aware of the most critical matters as they arise. We cannot attend to everything in our environment at once; that would lead to sensory overload and paralysis. The brain’s complex and constant monitoring of our internal and external environment is conducted automatically and unconsciously, only reaching our awareness as an emotion when the amygdala has assessed an immediate threat and has called upon some action by the body or intellectual faculties to address it. (It is a pickpocket!) Thus the limbic system is the neural mechanism pivotal in all social behaviors.
The amygdala receives sensory information from higher-order areas of the cerebral cortex. Different senses enter the amygdala through different pathways; for example, auditory information reaches the amygdala through the medial geniculate body. Knowing the anatomical name is not as important as understanding the concept of how different sensory abilities feed into the amygdala through separate lines of communication. The amygdala is like the Pentagon with its hotline to the White House (cerebral cortex). Other connections link the amygdala to the frontal lobe, which is where higher executive functions are carried out—functions critical to any threatening situation. Other fibers connect to the lower brain regions to control hormones, autonomic responses, and to the brain’s “relay center,” the thalamus, for sending sensory information up to the cerebral cortex. Controlling this relay center is how the amygdala brings specific events in our environment and internal states to our conscious awareness and filters out others. For example, pain is suppressed in the midst of a life-or-death battle. General anesthesia removes pain by preventing the cerebral cortex from responding to the signals streaming into our brain through pain fibers. If the signals never reach the cortex, we do not feel the pain, which explains why a soldier in battle can suffer a serious wound with no pain or conscious awareness of the injury: The amygdala has signaled the thalamus to cut off pain signals to the cerebral cortex, which enables his conscious faculties to fully engage with the life-risking threat. One can also see how dysfunction in the limbic system can lead to mental illnesses that affect emotion, threat responses, and antisocial behavior—illnesses such as mania, obsessive-compulsive disorder, or psychosis.
Humans depend most heavily on their sense of vision, but to most animals the world is experienced as a complex and dynamic realm of smells. The olfactory system connects to the limbic system, but not for analysis of an odor, but rather to evoke the emotion that is associated with it. The smell of smoke provokes alarm, the smell of food provokes hunger, and the smell of rot provokes repulsion, for example. The strong feelings evoked by specific odors are what give the sense of smell such power over us. Can you eat anything with the smell of vomit in the air? Could you sleep peacefully at night with the smell of smoke seeping from your attic? In most mammals, specific odors will trigger complex social interactions, including violent aggression.
“Septum” means wall of separation, or partition. In neuroanatomy, it refers to the thin membranous tissue that separates the left and right fluid-filled ventricles of the cerebral hemisphere. There are several clusters of neurons in the septal region, called nuclei. One of these clusters, the nucleus accumbens, lies just to one side of the septal nuclei. This is part of the brain’s reward system. This is the circuitry for the positive reinforcement we receive—the emotional boost, when we succeed at anything. Mood-enhancing drugs, such as cocaine, cause release of the neurotransmitter dopamine in the nucleus accumbens, delivering an artificially induced sensation of reward. Addiction to alcohol and other drugs involves changes in the nucleus accumbens reward system. As one would expect, the brain’s reward system plays a pivotal role in motivating a person’s behavior to seek novelty and danger or to shun them. The anxiety that grows into craving associated with drug and alcohol dependence is generated by changes in function in an addict’s nucleus accumbens that decrease dopamine levels. Similarly, general anxiety feeds through this same reward pathway in an individual confronted with the choice of taking a life-risking action or not.
When sensory information reaches the cerebral cortex, it is relayed to both the hippocampus and amygdala to rapidly assess whether the experience is novel or potentially threatening. The hippocampus links new sensations with memories of the past, looking for novelty and familiar rewarding experiences. The mundane is filtered out. Memory is not a video recording of sensory experiences; memory is very selective. In fact, memory is not a record at all but rather a mental reconstruction. This is why eyewitness testimony at trial and in general is so unreliable. By far, most of what we experience is rapidly forgotten. As we all know from personal experience, the emotional aspect of an event is a critical feature that determines whether an episode will be remembered. No one ever forgets a traumatic experience or any other emotionally charged event, even if it is encountered only once. You will never forget being mugged, for example; or your first kiss. Emotionally charged events are those the system identifies as having survival value and therefore need to be remembered to direct behavior appropriately in the future. It’s this interchange between the amygdala and hippocampus that filters out the noise of everyday existence, attaches emotion to meaningful events, and stamps the patterns of neural activity re-creating that experience in the mind to be retained for a lifetime if deemed important enough by this truly astonishing unconscious bit of our brain.
Now we pick up from where we first encountered blindsight, the ability of unseen visual stimuli to influence defensive behavior, which was described in the experiments on subjects who are blind in one eye but nevertheless are influenced by threatening faces shown to the sightless eye. Sensory information reaches the amygdala by at least two routes. One path is a direct line from the thalamus, because this is the shortest and fastest pathway from the body’s sense organs to the brain. This “subterranean” shortcut, tunneling beneath the cerebral cortex, is unconscious. We have no awareness of sensory information as it reaches the amygdala through the thalamus, but this high-speed communication route evokes rapid emotion and instantaneous reaction to a potential threat. The amygdala initiates this threat response by activating three neural circuits: First the amygdala stimulates the appropriate autonomic and endocrine systems located in the hypothalamus and brain stem to flood the bloodstream with adrenaline and stress hormones to trigger the fight-or-flight response or to evoke other profound emotional sensations from goose pimples to vomiting.
Second, the amygdala shoots information back to the hippocampus to reaffirm the emotional significance of what has simultaneously been sent there by other inputs. The message in English would be something like, This is important! Remember it!
Finally, both the hippocampus and amygdala relay signals to the cerebral cortex in the sensory association regions, where memories are made and context is synthesized and deliberation is added to set the body on a course of action. Now your conscious brain is being brought into the loop and you become aware that you are engaged in a threatening situation or defensive battle. We have already seen evidence of this in the study on people blinded in one eye from damage to the visual cortex who nevertheless demonstrate a heightened response to threatening images shown to the blind eye.
The second route into the amygdala is “aboveground,” through the cerebral cortex, where sensory input is relayed from sense organs and then analyzed in detail to extract intricate information and meaning, such as where the object is, what the object is, and where the object is going. Complex circuitry in the cerebral cortex makes associations among all of one’s senses, and cogitates on the significance of it all. This enormous computation requires a great deal of processing time, and in a sudden life-threatening situation, such as a rattlesnake strike, this route to action would be far too slow. However, this slower route to the amygdala can provoke the same reactions as the “subterranean” route, but it does so in response to far more complex environmental situations. One can also work themselves into a state of fear by this cortical pathway, as kids do when they tell ghost stories around the campfire.
It also works the other way: Picture a world-class rock climber as he creeps precariously up an impossibly sheer granite face on dime-edge footholds. As he does so, he starts to hum the scarecrow’s theme from The Wizard of Oz, “If I Only Had a Brain”:
doo da doot da do do doodo
da doot da doo doo doodo
da doot dooo do da dooooooo
The neurocircuitry for singing resides, of course, in the cerebral cortex. The pathways from the cerebral cortex to the subcortical fear- and threat-detection circuitry can suppress fear as well as reinforce it. The fear circuits are screaming up to the conscious brain, We’re gonna die! We’re gonna die! Singing, a “positive attitude,” and especially humor, puts a damper on the unconscious fear and rage circuitry to allow a person to maintain control (the proverbial whistling in the dark).
Yes, I know it’s sketchy, the cerebral cortex tells the amygdala by singing in response to those gut-twisting emotions that the mute unconscious brain is frantically pumping as panic up to our conscious mind, but I’ve got this.
The descending input from the cerebral cortex as it regulates the threat-detection circuitry is the neuroscience behind the iconic casual understatement and gallows humor of those who must operate in the most treacherous situations. Rodeo cowboys, adventurers, and men and women in the military all use these techniques to positive effect in order to operate in the most life-threatening conditions.
In Marcus Luttrell’s book Lone Survivor, he recounts a tale of awe-inspiring bravery in a horrendous battle in which his teammates were caught terribly outnumbered and surrounded by Taliban forces. Luttrell and the handful of SEALs decimated the enemy with skill, determination, and bravery, but the battle left only one of them alive. Luttrell’s account is replete with examples of the mechanism of cortical control of fear circuitry to persevere and succeed in a situation where all but the most elite among us would cower.
After jumping off a cliff to escape being blasted by bullets and RPGs (rocket-propelled grenades), Luttrell describes how his buddy Mikey Murphy recovered from the leap of faith amid the ricocheting bullets and deafening explosions:
He still had his rifle strapped on. Mine was resting at my feet. I grabbed it, and I heard Murphy shout through the din of explosions, “You good?”
I turned to him, and his entire face was black with dust. Even his goddamned teeth were black. “You look like shit, man,” I told him. “Fix yourself up!”
Despite everything, Mikey laughed, and then I noticed he’d been shot during the fall. There was blood pumping out of his stomach. But just then there was a thunderous explosion from one of the grenades, too close, much too close. . . .
SEALs never give up. Never. It is cortical control of their fear and rage circuits that helps them to persevere.
Later, after most of Luttrell’s team are mortally wounded but still 100 percent in the battle, firing their rifles and killing the enemy as they themselves lay fatally injured and trapped:
Mikey worked his way alongside me and said with vintage Murphy humor, “Man, this really sucks.”
I turned to face him and told him, “We’re gonna fucking die out here—if we’re not careful.”
“I know,” he replied.
And the battle raged on.
As described in Mark Owen’s book No Easy Day, running practical jokes, like the purple dildo that keeps cropping up in the team members’ gear at unexpected times and places, and the bra strap slipped onto the author’s backpack by a teammate as they escape from Osama bin Laden’s compound, were commonplace. They served to take the edge off so that the team could operate under stresses and dangers that few of us can easily imagine.
An important point about the sensory input to the subcortical pathway is that while the information is transmitted to the threat-detection circuits at the highest rate through this shortcut path, this pathway can convey only the most rudimentary information—the minimum that is necessary to alert us to danger. In receiving visual input from subcortical pathways to the amygdala, we cannot perceive an image. Forming an image would require far too much information processing that must pass through layers of cerebral cortex and reach many different cortical regions, but the amygdala does not need to form an image to exploit visual input for threat detection. Like a motion detector in a burglar-alarm system, which rapidly switches on warning lights and alarms when an intruder moves into range, the amygdala will do the same when an object—be it a baseball or a person’s fist—zips into your visual field and you jump to safety as you simultaneously duck and raise your hands in defense. Even though you can’t see it as anything more than a blur, that thing—whatever it is—suddenly appearing in your visual field should not be there. The object has violated your perimeter of safety and you are under threat. You will dodge and strike at it instantly, despite the fact that this is an extremely complex and highly coordinated sensory-motor response. Likewise for auditory input. In a scary movie a sudden bang causes you to jump even though you can’t discern if the sound is a gunshot, a slammed door, or an innocent hammer striking a nail. That abrupt loud sound could herald impending doom. There is no time to think. There is not even time to perceive the sound clearly. React! Kick the heart into high gear! Clench muscles for maximum strength! The sensory signals take the subterranean shortcut to the amygdala while they simultaneously split off and head toward the longer pathway into the cerebral cortex. Let the cerebral cortex catch up afterward and inform you of what the potential threat was that you have just avoided.
As I mentioned in chapter 1, dramatic pioneering research by Walter Rudolf Hess using electrical stimulation of the hypothalamus showed that there are automatic circuits of rage and aggression in the brain and that these “attack areas” reside in the hypothalamus. However, stimulating brain tissue with electrodes is not very precise. An electric shock spreads broadly, exciting larger areas of brain tissue and also activating nerve fibers that pass through the area from distant regions. Stimulating fibers of passage can lead to an incorrect conclusion about where the neurons that control a certain brain response are located. Modern methods are providing a much more detailed map of brain circuitry, and one of the fascinating discoveries is that different automatic attack behaviors are controlled by specific subregions of the hypothalamus. Very discrete circuits within the hypothalamus, amygdala, and other brain regions are involved in rapid responses to threat, and they are activated by very different types of threats. That is, the LIFEMORTS triggers have a corresponding and highly tuned circuit for each trigger.
Let’s have a look at the Family trigger as an example. This trigger circuitry, responsible for “momma bears” and superwoman confrontations with subway trains to protect their young, was identified by neuroscientists in 2014. Research on lab rats and mice has identified two specific subregions of the hypothalamus that are part of the maternal-aggression circuitry activated by the Family trigger. When a strange male rat is placed into a cage with a female rat tending her pups, the mother will immediately attack the male intruder. To identify the precise brain circuitry involved in maternal aggression, new and more fine-tuned methods than electrical stimulation are needed. One of these new methods allows researchers to see the activated circuits in the brain tissue with their own eyes.
Researchers use techniques that enable them to determine directly, by looking at brain tissue on a microscope slide, whether a neuron was firing rapidly just before the tissue specimen was taken for examination. In the 1990s researchers discovered that when neurons fire impulses, chemical signals reach the nucleus of the neuron to activate genes that are needed to make proteins in response to high levels of electrical activity. One of these genes is called c-fos. This gene makes a protein called Fos that binds to specific DNA sequences to “turn on” other genes—that is, to start the process of making mRNA from the DNA genetic code, to then make a specific protein, such as an ion channel, or cell signaling molecule, to better cope with the high level of neural activity. C-fos and other genes that act in this way are called “transcription factors” because they start the process of transcription (synthesis) of mRNA from the DNA template. Only genes that need to be turned on when a neuron fires rapidly have the DNA binding sites that Fos will recognize and bind to. This explains in part how the right genes out of the tens of thousands of genes in the cell’s nucleus are activated by the right stimulus. So when scientists see c-fos protein being made in a neuron, they know that this neuron was firing rapidly just before they took the brain sample to examine on a microscope slide. It is possible to see the amount of Fos in a neuron by using a staining technique that makes neurons stain darker (or shine brighter, if a fluorescent dye is used) in proportion to how much Fos is in the cell.
Neuroscientist Simone Motta and colleagues looked at the hypothalamus of a mother rat under a microscope just after a male intruder was placed in her cage with her and her newborn pups, which caused the mother rat to attack the intruder. Motta and her colleagues saw a specific spot in the rat’s hypothalamus that looked like it had been stippled with a black ink pen. These neurons here were loaded with Fos, meaning that the rat’s tiny collection of neurons had been firing rapidly in response to the Family trigger activated when the male intruded into her cage and provoked her to attack to defend her young.
These neurons were seen only in a small speck inside the hypothalamus, but when this tiny spot of neurons was surgically removed, the researchers found that the mother behaved normally in every other way, but attacks on male intruders ceased. (The brain is comprised of two symmetrical halves, the left and right, so this region had to be removed on both sides of the brain to fully abolish the mother’s protective attack response to a male intruder.) This spot resides in a general region of the hypothalamus called the hypothalamic attack area, which has been discussed previously in the pioneering experiments by Walter Rudolf Hess on initiating aggression in cats by electrical stimulation of this brain region. The spot itself is called the ventral premammillary nucleus (PMv). However, removing this tiny maternal aggression trigger spot in the hypothalamus does not affect other automated attack responses to different threats, as will be discussed. The PMv is part of the same Family trigger neurocircuitry that was likely activated in the mother moose’s brain when she suddenly attacked and killed Myong Chin Ra and later attacked Professor Bruno Kappes on the campus of the University of Alaska at Anchorage. It is not difficult to imagine how mothers, with different tendencies to protect their young or neglect them, could have corresponding differences in the PMv nucleus of their brain that controls the Family trigger.
By now you understand that no single part of the brain completely controls an animal’s aggressive response to a threat. The environmental triggers and the priming factors that change the threshold on when the trigger is activated are very complex, requiring threat detection and accurate response in complex social situations while the brain is engaged in countless other crucial tasks. The responses of aggression or retreat are also very complex behaviors, so many brain regions have to be engaged properly to launch an attack, freeze, or run.
Expecting that the amygdala must be involved in maternal aggression, not only the hypothalamus as just discussed, the scientists used the c-fos staining technique to discover if any part of the amygdala was also activated in the mother’s brain by the male intruder. Looking under the microscope they clearly saw two spots in the amygdala that stained strongly for c-Fos in response to activating the Family trigger. Both of these stained areas of the amygdala are known to receive input from the olfactory region. (These are the posteroventral and posterodorsal parts of the medial amygdalar nucleus [MEApv and MEApd], if you are a neurosurgeon or just interested in knowing the names of the exact spots.)
It makes perfect sense that aggression in rats can be triggered by olfaction, because the sense of smell is of primary importance to rodents. Rats and mice inhabit dark places and are nocturnally active, so their vision is not that good. Their senses of smell and touch through their whiskers are the most important senses for these rodents. Behavioral scientists had already shown that the smell of a male intruder was the prime trigger for launching aggression in mother rats. Cut the nerves from the nose to remove the sense of smell, and mother rats do not attack the male intruder. It is interesting that the PMv region of the hypothalamus, which is the linchpin of the maternal aggression response, has neurons in it that are known to respond specifically to odors only from the opposite sex. The whiskers also help a mother rat investigate an intruder immediately before an attack to defend her young.
Another part of the amygdala, the posterior amygdalar nucleus (PA) also showed strong staining for c-Fos. Neurons in this region are known to have receptors for stress hormones (mineralocorticoid receptors). Interestingly, when these stress hormone receptors are blocked in aggressive male rats, the animals become docile. This circuitry in the amygdala must link hormonal stress to the Family trigger circuitry, explaining in part how other aspects of a given situation, such as stress or hormones, can lower the threshold for pulling a specific trigger for rage. “There are always other factors,” Secret Service Agent Scott Moyer says concerning when people snap and commit a crime.
Likewise, another extension of the lateral amygdala, the BSTv area (bed nuclei of the stria terminalis), which is also activated in maternal aggression, has receptors for adrenaline and it receives input from the forebrain, which is the brain area associated with worry and deliberation. The BSTv also has connections to the hypothalamus that control autonomic responses and the release of hormones that control stress, mood, and anxiety. (Those hormones include oxytocin, corticotropin-releasing hormone, thyroid-stimulating hormone, TSH-releasing hormone, somatostatin, and dopamine). The BSTv is therefore in a position to strongly influence aggressive behavior and neuroendocrine responses involved in maternal aggression. Hormonal stimulation of this brain circuitry is the basis for the “roid rage” response in bodybuilders who take testosterone to build muscle mass and experience sudden rage as a side effect.
Looking more broadly throughout the brain, the researchers also saw other spots activated in circuits that would be necessary for the maternal aggression response. This included three other regions of the hypothalamus: (1) the medial preoptic nucleus (MPN), (2) the ventrolateral part (anatomical terminology for lower and to the side) of the hypothalamus called the lateral hypothalamic area (VMHvl), and (3) another spot to the side of the hypothalamus called the lateral hypothalamic area (LHAtu). Also a nucleus in the septal region (bed nuclei of the stria terminalis, BSTv) showed c-Fos staining. Importantly, the researchers found in rats that when the first spot that was identified in the hypothalamus was surgically removed (the PMv), the other spots were not stained for c-Fos (that is, marked as active) when a male intruder was present, which meant that the PMv is “upstream” of the other brain regions activated in maternal aggression.
It is important not to let the Latin tongue twister names get in the way. They are just geography; as is true for the Left Bank, the Eiffel Tower, and the Arc de Triomphe, until you become familiar with the geography, the names don’t mean much. But the conclusion from this research is not a difficult concept. The important thing to understand is that there is a specific circuit for maternal aggression in the unconscious brain and that the behavioral response is triggered by one spot, the PMv in the hypothalamus, that is particularly sensitive to a male intruder.
LIFEMORTS Trigger Circuits
Drawing exact parallels from rodent brains and rodent behavior to human brains and behavior is difficult, but these newly identified circuits can be roughly extrapolated into the LIFEMORTS triggers of human fear and aggression in the following way: The Life-or-limb trigger is the defensive response to injury, which is associated with pain. If something or someone inflicts pain on you, you will immediately respond aggressively to prevent further injury. Similarly, animal aggression in response to attack by a predator also encompasses the Life-or-limb trigger to defend oneself violently.
Aggression among individuals of the same species is how dominance is established in animals, from fish to primates. In humans, with our unique ability to use complex language, verbal insult achieves the same purpose: the Insult trigger, as examined in chapter 4 on the claw-hammer homicide at Carderock. The Organization trigger (social order) also involves violence within the same species to maintain social order. Not all animals are highly social, but those that are utilize violence to maintain compliance with social rules. Fear and threat circuitry activated by members of the same species (conspecifics) in animals, provokes anger and violent responses in human brains when other people do not follow social rules—if they don’t stop for a red light or cut in line, for example. We have already considered the Family trigger to protect one’s family in our discussion of animal research on maternal aggression.
The amygdala has several subregions, which we will refer to simply by their initials: L, BL, BM, ME, and CE. (For those interested in neuroanatomy, these correspond to lateral amygdala, basolateral amygdala, basomedial amygdala, medial amygdala, and central amygdala.)
A brief primer on the neuroanatomy of the amygdala will be helpful in understanding the fear and threat-detection circuitry in this brain region. The amygdala is an almond-shaped lump of tissue deep inside the temporal lobe of the brain. The amygdala looks different depending on how you slice through it, but in looking face-on at an MRI of the human brain at a slice through the top of the head, shoulder-to-shoulder, taken at about the level of the ears, the amygdala looks like a pair of narrowly spaced eyes, framed by the temporal lobes on the left and right sides of the brain. Each of the ingoing and outgoing connections in the amygdala forms a small knot of neurons, and these are clustered at different spots inside the amygdala. Early anatomists could clearly see these neuron clusters in their microscope slides, but they named them long before the function of any of these hubs of communication in the amygdala was known. So, unfortunately, the names (and the initials we use to refer to them) reflect little more than their location inside the amygdala. Thus we have central, lateral, and medial nuclei (clusters of neurons), as well as nuclei that sit in transitions between zones and in subdomains within zones; for example, basolateral (lower-left), and centromedial nuclei (in the middle of the middle!).
By analogy, one can view the amygdala as a map of Manhattan. The different nuclei correspond to different neighborhoods, and neurons correspond to individual buildings. Like police tracing a phone call to a specific building in the city, neuroscientists want to trace circuits to find the specific neurons responsible for fear and threat-detection inside the amygdala. The island of Manhattan is a tongue of land bordered on the west by the Hudson River and on the east by the East River. The streets of Manhattan are laid out in a gridwork pattern, numbered from near the tip of the tongue (southern extreme) sequentially to the base of the tongue (northern extreme). Major avenues run from north to south. Fifth Avenue splits midtown Manhattan into East Side and West Side, numbering from First Avenue on the East Side to Eleventh Avenue on the West Side.
This gridwork divides Manhattan into general regions, which is helpful in communicating your desired destination to a cabdriver, for example. “Uptown” refers to property above Fifty-Ninth Street. Central Park, a rectangular green space, is situated at the core of Manhattan, as its name suggests. “Downtown” refers to the tip of the tongue below Fourteenth Street. By analogy, the basolateral nuclei (BL) of the amygdala might correspond to the West Side of Manhattan, the central medial nuclei to Central Park and the Upper East Side of Manhattan; the dorsal amygdala would correspond to Northern Manhattan.
Manhattan is further divided into subregions of smaller neighborhoods, each of which has its unique identity and boundary, but the names themselves tell you nothing about the character of the neighborhood; they are just labels. For example, Harlem is an uptown neighborhood, and Greenwich Village is one of the downtown neighborhoods. Likewise in the basolateral region of the amygdala there are smaller neighborhoods (nuclei). For example, there’s the lateral nucleus (L), basal nucleus, accessory nucleus, and others, and in the centromedial region of the amygdala we have the central (CE), medial (ME), and bed nucleus of the stria terminalis (BNst).
This is a lot of terminology to swallow, but it is not a difficult concept. Furthermore, the terminology can be confusing because different people may refer to the same spot by different names. Just as New Yorkers sometimes argue over whether a neighborhood should be called Hell’s Kitchen or Clinton, so too do neuroanatomists like to quibble sometimes over anatomical names. There are, however, many more neighborhoods in Manhattan than named nuclei in the amygdala, so it doesn’t take a brain surgeon to learn their names if you want to consult a neuroanatomy book. However, for present purposes it is not necessary to learn the names of any of the various “neighborhoods” in the amygdala. The important point is that different LIFEMORTS triggers connect through different circuits passing through different communication hubs in the amygdala. From these points the circuits interconnect with other brain regions, such as the cerebral cortex and hypothalamus.
In rodents, response to predators is conveyed through connections from the olfactory system to the ME, L, and BM nuclei of the amygdala. By analogy, this roughly corresponds to Midtown and the Lower East Side (ME), the West Side (L), and somewhere around the Greenwich Village / West Village region (BM). These connections have been determined using methods like the ones that uncovered the circuitry for maternal aggression.
Fear that is learned, rather than innate fear, involves the lateral (L) region of the amygdala and causes us to associate certain cues with danger, much the way you’d learn that a certain part of your neighborhood is dangerous after dark. Damage to the L region of the amygdala prevents rats from learning that a certain part of their environment is dangerous. This is studied in the laboratory where rats learn that if they venture into certain parts of the test cage, they will receive a nasty electrical shock to their feet through the steel floor. Under normal conditioning they learn to avoid this part of the cage. The L region sends connections to the CE and to the BL. If drugs are used to block activity in the CE, rodents no longer exhibit fear in response to that area of the cage, but here’s an important point: The same animals still exhibit fear that they have learned to associate with predators. This shows that different fear and threat circuits are linked to different LIFEMORTS threat triggers in the brain.
Meanwhile, if the ME portion of the amygdala is blocked, rats exhibit exactly the opposite response to fear associated with predators versus foot shock. This shows that the fear-of-pain circuit and the fear-of-predator circuits are in different modules inside the amygdala. These parallel circuits for different types of threats extend beyond the amygdala; indeed, they span throughout a large network of brain connections.
In recent studies, researchers compared a rat’s brain responses to a predator—namely a cat—with its brain responses to another rat intruding on its territory. This parallels the Life-or-limb trigger for defense when the rat sees a cat, a dangerous predator, with the Environment trigger to defend one’s territory when the test rat sees another rat intruding into its cage. Researchers found that introducing a strange rat into the test cage activated the dorsal medial part of the hypothalamus. Electrical stimulation of this region in humans elicits panic attacks. However, when a cat is presented, a different region is activated—the ventral lateral part of the hypothalamus. When the scientists removed one of these two regions, either the fear response to only the Environment trigger (intruder; another rat) or the Life-or-limb trigger (predator; a cat) remained intact, depending on which brain region was surgically removed. This shows that the Life-or-limb and Environment trigger circuits are separate.
“We have also some findings regarding restraint,” Dr. Newton Canteras replied in response to a question I’d asked about the Stopped trigger of rage circuitry, “but they are still very preliminary.” Identifying the neurocircuitry for the LIFEMORTS triggers is at the cutting edge of neuroscience research, but it is clear that different threats activate very specific and distinct circuits. It is reasonable to assume that part of the reason people find different kinds of situations frightening and are provoked to sudden rage by different triggers is that the threat-detection and fear circuits responding to different types of threats are not developed to the same extent in everyone. Thus one person could be provoked by minor insults (Insult trigger) but have a slow fuse in responding to seeing other people violate social rules (Organization trigger), and another could have the opposite tendency.
Consider the output circuits from the amygdala that drive specific behavioral actions. A rat’s behavioral response to a predator and an intruder are quite different. The sight of a cat causes the rat to freeze in fear, whereas an intruding rat causes the resident rat to attack. Indeed, it’s two different pathways leading out of the hypothalamus that activate the periaqueductal gray brain region in response to these two different triggers. This information travels to the conscious brain to generate the sense of fear via connections from the periaqueductal gray to the thalamus and then reaches the cerebral cortex to bring awareness of the situation.
This line of research raises interesting questions, not fully answered by experimental studies at present, about whether individual differences in a person’s reaction to a threat—a mugger, for example—would depend in part on innate differences in the strength of these two circuits in different people. This would help account for how different people respond differently to an identical threatening situation—one person may freeze and the other may fight. Based on what we know about other brain functions and the circuit activity that supports them, this seems reasonable. It also seems reasonable to expect that the relative strength of the two circuits that control freezing or fighting in this experiment with rats and cats would depend in part not only on inherited genetic differences that guided the circuits’ development, but also on the individual’s life experiences, which could have strengthened or weakened either one. Extensive experience operating in the face of danger, such as a Navy SEAL who drills constantly under intense stress, or traumatic events in early life, might reasonably alter the balance of freezing or fighting in different individuals.
As discussed in reference to heart-rate variability, reflexive threat responses are modified by prefrontal inhibition of the amygdala, but information processing in the cerebral cortex can also activate the threat-response circuit (the “top-down control” we learned about in chapter 1). Recall what happened when terrorist Umar Farouk Abdulmutallab attempted to detonate plastic explosives concealed in his underwear on an airline traveling from Amsterdam to Detroit on Christmas Eve, December 24, 2009. Suddenly there was a loud pop and smoke billowed up from one of the passengers on Northwest Airlines Flight 253. Everyone surrounding the person fled for safety, but one passenger—Jasper Schuringa—instantly leaped over rows of seats to tackle the underwear bomber and put out the flames with his bare hands, subdue the terrorist, and thus save every person on that airplane. Why did he react this way when everyone else had the opposite response and probably the most natural reflex to a loud noise and smoke—to flee? Is it that Schuringa is preprogrammed to attack a threat, whereas others are preprogrammed to flee? In part this is likely, but a Navy SEAL that I asked points out another factor, based on his own training and experience responding immediately to countless life-risking threats. Situation analysis in the cerebral cortex to engage the defense reflex (top-down control) could have been an important factor in this incident:
“I think the guy who reacted that way understood the situation. ‘Hey! I need to act offensively or something’s going to happen.’ Everybody else in their mind thought, ‘I need to get out of here to protect myself.’ They didn’t understand the bigger significance of the threat. Somebody smoking [from a bomb] on an aircraft—that’s not good for anybody on the aircraft.”
SEAL training places great emphasis on rapid analysis (cortical activity) to activate appropriate subcortical reactions to threats.
“It is one thing if we’re on the street and some guy’s cooking off a bomb a hundred yards away; I’m not gonna go running over to him, I’m just gonna get everybody to back away and he can blow himself up. That’s fine, but in an aircraft, I would say that person had the cognizance to think, ‘If I don’t act, everybody including myself is done.’
“Break that entire situation down and assess. A lot of people who might have fled might have been women and kids who assessed that ‘Hey, I can’t do anything if I tried. What am I going to do to this much bigger guy if I tried?’ Whereas maybe that guy who dove on him had something in his past, some training—sports, or something where he understood he needed to act offensively in that moment.”
Clearly the “lizard brain” simplicity of the past century has had its day. Much of this threat-assessment analysis utilizes the cerebral cortex. So does analyzing a complex social threat such as an intruder entering one’s environment. The cerebral cortex is an essential part of the threat response.
To Fight, Freeze, or Flee
A mouse is roaming around its cage curiously, sniffing and wiggling its whiskers, but there is a slender fiber-optic cable coming out of its head connected to a bank of electronic equipment. Suddenly a blue flash of light from a laser illuminates the fiber-optic cable and the mouse freezes instantly as if it had encountered a cat. Light-sensitive ion channels have been genetically inserted into specific neurons in the mouse’s brain. When these channels are activated by blue light, they cause the neuron to fire electrical impulses. This method of stimulating neurons (optogenetics) is superior to using electrodes to stimulate brain tissue, because the light-sensitive channels can be inserted specifically into only the neurons that the researcher is interested in exciting without having the stimulation spread to other areas. In this case, optogenetics is being used to uncover the function of neurons in a particular spot in the amygdala. Other light-sensitive channels can be used that inhibit electrical firing of neurons. This particular mouse has had these ion channels inserted genetically into neurons in the CM region of its amygdala. With the flick of a light switch, we know precisely what behavior these neurons control. Neurons in the CM region of the amygdala cause the mouse to freeze in fear. These neurons send their signals out of the amygdala to the brain stem—in particular the periaqueductal gray area. Thus they are the action channel—or output path from the amygdala—for freezing in fright.
A subcircuit in the periaqueductal gray (PAG) called the ventral lateral nucleus is where these amygdala outputs that cause freezing send their signals. From there, signals go out to other regions of the brain, controlling movement by activating motor axons that run down the spinal cord and eventually out to the muscles. This causes the muscles to clench and the animal to freeze. A different subcircuit in the PAG is responsible for the opposite response—attack. That’s what the rat will do instantly when the fiber-optic light stimulates these particular neurons located in the dorsal lateral nucleus of the PAG. Scientists have control of fight or freezing by tapping into the appropriate circuit. When they stimulate these cells optogenetically, the mouse begins to frantically run in an attempt to flee, as if seeing a ghost. Scientists can activate this region of the PAG on either the right or left side of the animal’s brain, and this causes the mouse to run in circles—either clockwise or counterclockwise, depending on whether the left or right PAG flight neurons are stimulated.
It is interesting to note that the PAG is also an important structure in pain signaling. (Recall our discussion in chapter 1 that just as New York City is the financial capital of the United States, it is also the publishing capital. So too can the same brain region have more than one function.) An alternative hypothesis might have been that stimulating these neurons was causing pain rather than activating the flight behavior and instead the mouse was fleeing in an attempt to escape intense pain when researchers activated the neurons with the laser. But tests of pain threshold in these animals proved exactly the opposite. Stimulating the neurons that cause the mouse to flee in fright also caused a powerful analgesic effect, strongly inhibiting the sensation of pain. This was tested harmlessly by dipping the mouse’s tail in hot water and measuring how quickly it flicked it away, depending on how hot the water was. The circuitry that combines threat and pain circuits explains how pain is suppressed while fleeing in fear.
The scientists also engineered a protein into neurons of interest so that they would emit light when they fired. The researchers were able to watch these neurons flash through a fiber-optic cable inserted into the brain and magnified by a microscope as the animal reacted to threats. The scientists saw these freeze-or-flee neurons in the PAG flash when the mouse was provoked to either freeze in fright or to flee.
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We have now dissected the rage circuitry in the brain, explored at a cellular level how it works, and seen how essential this circuitry is to our life in a positive way, but also how these circuits releasing sudden aggression can become activated inappropriately, often with regrettable outcomes. In the next part of the book we look beyond the individual. How do the circuits in our brain that control sudden aggression and violence affect societies and other interpersonal relationships—from couples, families, and coworkers to global politics? All of these interactions are profoundly affected by the neurocircuits of snapping and aggression, both in essential ways to maintain cooperation and peace among people and in regrettable instances where these interpersonal relations become dysfunctional and result in sudden conflict. The scope of interpersonal relations will bring us now to examine closely two of the most powerful triggers of rage in the brain of our species: the Mate trigger and the Tribe trigger of aggression.