[Buddha-l] The Amygdala and Fear

[S.A. Feite]

Some interesting background material on the amygdala from an academic Neurologist, meditation researcher and an advanced dharma practitioner.

From: 

_Zen and the Brain_
James Austin, MD

Chapter 41

_The Amygdala and Fear_

Rage, rage against the dying of the light . . .

Dylan Thomas (1914–1953)1

No man is free if he fears death.

Martin Luther King, Jr. (1929–1968)2

In the two previous chapters, we began to make loose and qualified associations,
relating certain deep anterior midline regions to some of our positive, energized,
pleasurable states. Now, the amygdala introduces us to our brain’s negative valences.
These are the sources of our burning, raging fear of death. The amygdala,
too, gets its name from its shape: like an almond. Each amygdala is an extended
ovoid mass of gray matter buried near the inside tip of the temporal lobe. Collectively,
its several nuclei are now called the amygdaloid complex. An accurate
term, in view of its other complexities.

A brief survey of its anatomy helps us understand what the amygdala does.
Vital subcortical input comes over to it from the mediodorsal nucleus of the thalamus
and speeds up from the ventromedial hypothalamus. Impulses descend to
it from the cortex of the anterior cingulate gyrus, the prefrontal, orbitofrontal, and
the temporal regions. The amygdala then gives rise to two major outflow paths.
Its upper path leads back to the ventromedial hypothalamus. The lower pathway
curves down to inform the brain stem and the base of the brain.

As hominids evolved, they left us many legacies. One was an amygdala
whose basal and lateral nuclei had become very large, but whose corticomedial
and central nuclei had become relatively small.3 Many kinds of peptide nerve
endings funnel into these smaller nuclei, but the opioid peptide terminals are dispersed
more evenly.4

Sensate messages filter down to the amygdala from the association cortex
only after they have been highly processed. And as these cortical messages descend,
they pass at each step through a series of synapses increasingly invested
with acetylcholine terminals and opioid receptors.5 So the closer our layers of
sensory associations draw to the limbic system, the more they can be influenced
by cholinergic and opioid receptors.

The amygdala itself contains sophisticated wiring patterns. These add critical
physiological implications to all the other cited architectural features at the
interface between the temporal lobe and the limbic system. For example, the circuitries
of its large basolateral nuclei already resemble those of a cerebral cortex
in miniature. This suggests that the amygdala could be competent to insert emotional
resonances, either positive or negative, which further color the meaning of
our higher-order associations.

Consider further the interesting findings in certain cats who happen to have
been born defensive and easily frightened. What makes them different when they
encounter threatening stimuli? These timid cats generate the most activity in the

41. The Amygdala and Fear 175

pathway connecting the amygdala to the hypothalamus.6 Moreover, the normal
basolateral amygdala has options for relaying another set of messages to both the
dorsal and ventral striatum. Over these other output pathways the amygdala can
instantly insert its bias into our affective behavior.7–9

The amygdaloid complex is relatively small. Are we so sure it contributes
to behavior? Could it really be helping us smile or frown? Such questions prompt
us to reflect on Herbert’s caveat: “We must overhaul our methods of studying
behavior if we are to make functional sense of the new knowledge about the
structure and organization of the limbic system.”10

True, earlier electrical stimulations of the amygdala in animals did cause
different kinds of behaviors. They included fearful, ragelike, and defensive reactions,
autonomic and endocrine responses, plus simpler arousal responses. But
the stimuli were gross, and so once again one must discount the results of most
of the earlier stimulation research. Moreover, when lesions were made they were
too large. They also cut fibers passing through the amygdala on their way elsewhere.
In contrast, the newer generations of smaller lesions yield results much
more interpretable. They are made by injecting local excitotoxins. These chemical
lesions selectively destroy intrinsic nerve cells, but they spare the extrinsic axons
on their way to and from other regions.11 Excitotoxic lesions have interesting implications
(see chapter 152).

Meanwhile, we still need to overhaul the ways we study behavior. First, how
shall we define it? Always in terms of action? Sometimes inaction is an impressive
form of behavior. To explore such possibilities, let us begin by observing a dominant
rat who regards his home cage as his castle. He possesses it and marks it.
He defends his cage as though it were a part of himself. On the biological high
ground of his very own turf, he is action personified. This owner rat is a “winner.”
He always defeats a normal intruder rat. Let us then turn our sympathies to the
intruder rat, as one does to an underdog. How does this second rat behave, after
being defeated, when we return him to his own home cage next door? There he
stays quiet, “frozen” in his corner. This vanquished intruder is “once bitten, twice
shy.” Never will he venture over even to sniff at, let alone to challenge, the victor
who goes on patrolling the boundary of his own nearby castle-cage.12
Now, suppose we bring in a third rat. He too, will be cast in the role of the
intruder. But one small aspect of his behavior has been modified. A very discrete
lesion has already been made in this third rat’s corticomedial amygdala. At first,
he seems normal. Indeed, he still fights just as hard, because this tiny lesion won’t
change his gross combative behavior either before, or during, his inevitable defeat.
But observe how he behaves after being defeated. Now one sees that this
latest, lesioned intruder differs strikingly from the normal intruder. He moves
freely about his own cage. He even thrusts his muzzle out though the wire of his
cage, sniffing incautiously toward the victorious rat. Had this third rat really been
in, and lost, the battle? You’d never guess it. He seems oblivious of the proprieties,
of his expected social boundaries. He hasn’t learned his lesson.
No naivete of this degree will help any creature adapt to surroundings that
are always hostile and competitive. But taking this experiment as a clue, we might
simplify one aspect of the normal functions of the medial amygdala as follows:

176 III. Neurologizing

it contributes to survival skills, to behaviors that in the inner city one might call
“street-smarts.” Taken together, the smaller corticomedial and central amygdala
also participate in those systems mediating basic drives. What enables them to do
so? Note again those outflow paths projecting messages into the hypothalamus,
striatum, and the brain stem.13,14

Earlier generations relied on the active practice known as “spare the rod
and spoil the child.” Did the amygdala enter into this adage? Probably. For the
amygdala does seem to be a major factor in aversive learning experiences. These
are the kinds of learning which depend on negative, highly arousing, stressful,
or otherwise unpleasant circumstances. Did the amygdala even take on the contrasting
role, the one implicit in the old “carrot-and-stick” approach? Probably,
even if it is a lesser one. For it also fosters positive learning experiences. These are
the kinds that occur when appetitive, food-and-drink reinforcements are added.
These are the “carrots” that enhance learning.15

When researchers use the “stick” approach, they can aversively condition
rats to fear a pure tone. They begin by delivering this tone along with a mild foot
shock. Soon, just the tone alone causes the rats to “freeze,” and it increases their
heart rate and blood pressure. Suppose, however, that lesions had been made
earlier in the lateral amygdaloid nucleus. They prevent these fearful autonomic
and behavioral responses. So this lateral nucleus is an essential earlier interface
in conditioning.

When sound stimuli arrive at the lateral nucleus, it then relays its signals on
to the central nucleus. The central nucleus then becomes the next link in the chain
of “emotionalizing” circuitry that underlies aversive conditioning.16 Finally, when
the central nucleus exports such messages, it will be preparing the animal to
respond to the impending stressful event.14

Suppose you place lesions at a much higher level, far up in the conditioned
rats’ auditory cortex. Do lesions this high stop the sound from entering, and stop
the tone from causing fearful behavior?17 No. Already the brain will have shunted
in, lower down, those pivotal sensory signals crucial for comfort or survival. Indeed,
it will have mobilized them into its behavior long before.18 Everyone knows
by now that mere high-minded thoughts won’t banish deep fear and rage.
Up to now, we have been observing how learning takes place in adult rats.
These adults have learned to fear through the process of conditioning. But the
amygdala had been primed long before. It was already genetically programmed
to help generate primal fear. A normal rat innately fears a cat. Seeing a cat, it
freezes. However, rats lose this instinctive fearful behavior after they have had
lesions of the amygdala. They will even climb up on the back of a sleeping cat
after you have rendered the cat harmless with a hypnotic drug.19

Can one create a functional block in the amygdala, banish fear without actually
destroying nerve cells? Yes, researchers can inject two kinds of drugs directly
into the amygdala to reduce a rat’s anxiety behaviors. This approach takes advantage
of an important fact: the normal amygdala is loaded with receptors sensitive
to opioid drugs and to other antianxiety drugs. When we humans tune down and
resolve many of our own anxious fears, it seems likely that we will be using these
same two kinds of receptors.19

41. The Amygdala and Fear 177

Rats are paranoid about new tastes and smells. Rats not suspicious about
what they might eat dropped out of the gene pool long ago. Today’s survivors
have hardwired such phobias into their brains. The basolateral amygdala normally
contributes to this innate tendency to fear any new taste. It also helps the rat
further condition its already keen aversion to certain odors. But after having small
lesions made in their amygdala, the rats no longer recoil from a novel food in a
novel environment.11 In primates, too, novel stimuli prompt many nerve cells in
the amygdala to fire vigorously.20

Then what about the “carrot” approach? Now, the amygdala responds “positively.”
Its small central nucleus seems to lend “seasoning” to some of these
positive resonances, flavoring the brain’s appetitive memories for food.13 On the
other hand, studies in cats show that the central nucleus can also enter into the
visceral counterparts of fear. For cats can be conditioned to become fearful by
using a variety of techniques that follow the “stick” approach. Their blood pressures
rise, and they breathe faster. However, these elevated blood pressures fall
and breathing rates slow after their central nucleus has been inactivated.21,22 In
fact, an effective way to suppress a fearful cat’s brief “hair-on-end” reaction is to
inject an enkephalin opioid into the amygdala’s upper output pathway.23,24
When an awake animal breathes in, many of its amygdala nerve cells discharge.
In contrast, while exhaling, only half that number fire. Fewer still fire when
the animal enters quiet sleep or REM sleep.25 Such findings reemphasize an important
point cited back in chapter 22. Not only does meditation affect breathing;
breathing can go on to influence meditative experience. More specifically, expiration
quiets down the firing of the central amygdala.

Different Kinds of Aggressive and Fearful Behaviors

A poet, sensitive to the ultimate roots of rage, is only one illustration of the broad
scope of aggression. Aggression takes many other forms, and the early years of
meditative training can modify only some of these.

As noted earlier, cats can be prompted into a very aggressive attack when
electrical stimuli are directed into the hypothalamus.26 Suppose, however, the researcher
first destroys the amygdala on both sides. Now, despite the stimuli to
the hypothalamus, it becomes more difficult to drive these various kinds of attack
behaviors. Yet, even though these lesioned animals do become calmer, they have
arrived at only a temporary serenity. How can one bring back their attack behavior?
By stimulating them with a dopamine agonist.27 Such relapses imply that
aggressive behavior is not going to stop if one merely reduces the relevant functions
of the amygdala per se. At a minimum, one also needs to reduce certain
dopamine and hypothalamic mechanisms as well.

Most of the evidence presented so far has come from research models in
lower animals. What about the heart-pounding rush of fear in primates more like
ourselves? When Brown and Schafer studied primates, over a century ago, they
discovered a surprising fact. They could tame wild monkeys if they removed the
temporal lobes on both sides.28 Today we know that one critical feature responsible
for this “gentling” process is the loss of the amygdala. Indeed, monkeys do
become “strikingly fearless” after both their right and left amygdalae have been

178 III. Neurologizing

removed. So naive, in fact, that they will approach and handle a snake! No normal
monkey comes near a snake.29 These monkeys’ fearless, incautious behavior resembles
that of the lesioned rats and cats.

Even so, the lesioned monkeys still show a few lingering traces of fear behavior.
Suppose you place them in different, fear-provoking situations. Then, a
few of their facial expressions and postures still reveal fearful or submissive behaviors.
Where might these come from? Some of the responsible visual messages
normally enter from the nearby inferotemporal cortex.30 Elsewhere, on the output
side, such lingering fearful behaviors might also reflect the way that dopamine
systems keep exerting their same persistent influence, noted above, when DA
activates the nearby motor circuits of the striatum.

Clinical studies of humans confirm that the amygdala is a major primary
nodal point when we consciously experience fear. When it is stimulated selectively,
the subjects experience mental tension and behave in a tense manner.31 In
one such patient, stimulation immediately induced fear. Fear later came back
when the afterdischarges spread back into the amygdala on return from the hippocampus.
32 Moreover, one other patient had recurrent episodes of spontaneous
fear lasting minutes to hours. These fears were prompted by an epileptic focus
that was discharging into the right anterior temporal region. The fearful episodes
ceased when the amygdala was removed along with adjacent parts of the medial
temporal lobe.33

As is also true of lower animals, the evidence that would link the human
amygdala with aggression is less consistent. “There can be both aggressive behavior
without limbic lesions and limbic lesions without aggressive behavior.”33 Neurosurgical
lesions aimed at the human amygdala sometimes relieve excessively
aggressive behavior, but sometimes they do not.34

Recent studies suggest that human subjects employ several different anatomical
pathways as they proceed to channel various kinds of emotions out into
the autonomic nervous system.35,36 Future research may tease out many subtly
different shadings of diverse human social interactions that can be influenced by
the subdivisions of our amygdala.37 Consider, as but one of these possibilities, the
effect that small lesions have on male rats. Corticomedial lesions reduce their
heterosexual behavior, but do not change they way they act aggressively toward
other males. In contrast, lesions of the basolateral amygdala reduce aggressive
interactions among male rats, but do not affect their sexual behavior toward
females.38

To summarize: Our amygdala enters early into a vital “loop” of incoming
signals. It comes instantly to conclusions about their survival or reinforcement
value. It then relays its biased affective valences on to other circuits. They, in
turn, will orchestrate the appropriate behavioral responses both instinctual and
learned, somatic and visceral. In addition, the amygdala is a nodal point for many
circuits linked to our primary experience of fear.