Shall we be Frightened or not?

Alan Challoner MA MChS

You encounter a rabbit whilst walking along a path in the woods. Light reflected from the
rabbit is picked up by your eyes. The signals are then transmitted through the visual system to
your visual thalamus, and then to your visual cortex, where a sensory representation of the
rabbit is created and held in a short-term visual object buffer. Connections from the visual
cortex to the cortical long-term memory networks activate relevant memories (facts about
rabbits stored in memory as well as memories about past experiences you may have had
with rabbits). By way of connections between the long-term memory networks and the
working memory system, activated long-term memories are integrated with the sensory
representation of the stimulus in working memory, allowing you to be consciously aware that
the object you are looking at is a rabbit.

A few strides later down the path and you come across a snake coiled up next to a log.
Your eyes also pick up on this stimulus. Conscious representations are created in the same
way as for the rabbit by the integration in working memory of short-term visual
representations with information from long-term memory. However, in the case of the snake,
in addition to being aware of the kind of animal you are looking at, long-term memory also
informs you that this kind of animal can be dangerous and that you might be in danger.

According to cognitive appraisal theories, the processes described so far would constitute
your assessment of the situation and should be enough to account for the fear that you are
feeling as a result of encountering the snake. The difference between the working memory
representation of the rabbit and the snake is that the latter includes information about the
snake being dangerous. These cognitive representations and appraisals in working memory
are not enough to turn the experience into a full-blown emotional experience. Something
else is needed to turn cognitive appraisals into emotions, to turn experiences into emotional
experiences. That something, of course, is the activation of the system built by evolution to
deal with dangers; and that crucially involves the amygdala.

Many people, but not all, who encounter a snake in a situation such as the one described
will have a full-blown emotional reaction that includes bodily responses and emotional
feelings. 1 This will only occur if the visual representation of the snake triggers the amygdala.
A whole host of connections will then be activated. Activation of these is what makes the
encounter with the snake an emotional experience, and the absence of activation is what
prevents the encounter with the rabbit from being one. 2

Neurons in the area of the thalamus that project to the primary auditory cortex are narrowly
tuned they are very particular to what they will respond. However, cells in the thalamic
areas that project to the amygdala are less particular they respond to a much wider
range of stimuli and are said to be broadly tuned. Music will sound the same to the
amygdala by way of the thalamic projections but quite different by way of the cortical
projections. So when two similar stimuli are used in a conditioning study, the thalamus will
1

send the amygdala essentially the same information, regardless of which stimulus it is
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1 Erdelyi, M H. The recovery of unconscious (inaccessible) memories: Laboratory studies of

hypermnesia. In The psychology of learning and motivation: Advances in research and theory,
G. Bower, ed. (New York: Academic Press), pp. 95-127; 1984.
2 If, in your past, you have experienced rabbits in association with some trauma or stress, then
the rabbit too could serve as a trigger stimulus that would turn on the amygdala and its
outputs.
processing, but when the cortex processes the different stimuli it will send the amygdala
different signals. If the cortex is damaged, the animal has only the direct thalamic pathway
and thus the amygdala treats the two stimuli the same both elicit conditioned fear.

Although the thalamic system cannot make fine distinctions, it has an important advantage
over the cortical input pathway to the amygdala. That advantage is time. In a rat it takes
about twelve milliseconds (twelve one-thousandths of a second) for an acoustic stimulus to
reach the amygdala through the thalamic pathway, and almost twice as long through the
cortical pathway. The thalamic pathway is thus faster. It cannot tell the amygdala exactly
what is there, but can provide a fast signal that warns that something dangerous may be
there. It is a quick and dirty processing system.

Thalamocortical pathways carrying vestibular information.

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Imagine walking in the woods. A crackling sound occurs. It goes straight to the amygdala
through the thalamic pathway. The sound also goes from the thalamus to the cortex, which
recognizes the sound to be a dry twig that snapped under the weight of your boot, or that of
a rattlesnake shaking its tail. But by the time the cortex has figured this out, the amygdala is
already starting to defend against the snake. The information received from the thalamus is
unfiltered and biased toward evoking responses. The cortex's job is to prevent the
inappropriate response rather than to produce the appropriate one. Alternatively, suppose
there is a slender curved shape on the path. The curvature and slenderness reach the
amygdala from the thalamus, whereas only the cortex distinguishes a coiled up snake from a
curved stick. If it is a snake, the amygdala is ahead of the game. From the point of view of
survival, it is better to respond to potentially dangerous events as if they were in fact the real
thing than to fail to respond. The cost of treating a stick as a snake is less, in the long run,
than the cost of treating a snake as a stick. (LeDoux, 1998, Idem)

So we can begin to see the outline of a fear reaction system. It involves parallel transmission
to the amygdala from the sensory thalamus and sensory cortex. The subcortical pathways
provide a crude image of the external world, whereas more detailed and accurate rep-
resentations come from the cortex. While the pathway from the thalamus only involves one
link; several links are required to activate the amygdala by way of the cortex. Since each
link adds time, the thalamic pathway is faster. Interestingly, the thalamo-amygdala and
cortico-amygdala pathways converge in the lateral nucleus of the amygdala. In all
likelihood, normally both pathways transmit signals to the lateral nucleus, which appears to
play a pivotal role in coordinating the sensory processes that constitute the conditioned fear
stimulus. Once the information has reached the lateral nucleus it can be distributed through
the internal amygdala pathways to the central nucleus, which then unleashes the full
repertoire of defensive reactions. 3

Fear Conditioning in Humans Human subjects do exhibit reliable conditioned

fear responses4,5,6 although these responses may be influenced somewhat by certain
personality characteristics7,8 and cognitive processes9. Despite its success in animal research,
fear conditioning has not been widely used in the neuropsychological assessment of human
brain function, where little is known about the neural basis of emotion.

It has been shown that, as in other species, the integrity of the medial temporal lobe is
important for conditioned emotional learning in humans, although assessment of the relative
contributions of particular structures within this region must await future investigation in
patients with more restricted damage and functional imaging studies in healthy adults.
(LaBar, 1997 idem) Fear conditioning paradigms have also been proposed as a model

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system for studying emotional processing in clinical populations with affective and traumatic

3 Johnson-Laird, PN. The computer and the mind: An introduction to cognitive science
(Cambridge: Harvard University Press; 1988).
4 Hodes RL; Cook EW & Lang PJ. Individual differences in autonomic response: Conditioned
association or conditioned fear? Psychophysiology 22: 545-560, 1985.
5 Grillon C; Ameli R & Woods SW, et al. Fear-potentiated startle in humans: Effects of anticipatory
anxiety on the acoustic blink reflex. Psychophysiology 28:588-595, 1991.
6 Fredrickson M; Annas P & Georgiades A, et al. Internal consistency and temporal stability of
classically conditioned skin conductance responses. Bioi Psychol 35:153-163, 1993.
7 Eysenck HJ. The conditioning model of neurosis. Behav Brain Sci 2:155-199, 1979.
8 Guimaraes FS; Hellewell J & Hensman R, et al. Characterization of a psychophysiological
model of classical fear conditioning in healthy volunteers: Influence of gender, instruction,
personality and placebo. Psychopharmacology 104:231-236, 1990.
9 Davey G (ed): Cognitive Processes and Pavlovian Conditioning in Humans. Chichester,
England: Wiley, 1987.
memory disorders.10,11

The amygdala has been implicated in aspects of fear regulation in both human12,13,14 and
non-human studies. 15 The amygdala also appears to be involved in stimulus reward
learning16,17 and may contribute to dysfunction characterized by other disorders of affect
(Aggleton, 1992, idem). Gray 18 has incorporated the septo-hippocampal system into a
behavioural inhibition model of anxiety and stress, with an emphasis on its role in cognitive
monitoring and coping strategies. This conception reflects how cognitive influences enter
into emotional networks and complements the investigation of the role of the hippocampus
in more complex aspects of conditioned fear. (LaBar, 1997, idem)

The integrity of the orbitofrontal cortex is critical for the appropriate adjustment of
behavioural responses to changing reinforcement contingencies, which may account for
some of the emotional deficits following frontal lobe damage 19. The orbitofrontal cortex may
also function as a link between internal somatic states and social perceptions in the
guidance of behaviour20, and prefrontal-cingulate-amygdala connectivity with effector
structures seems to be particularly important for mediating socio-emotional interactions.

Thus, particular structures of the limbic forebrain appear to play distinct roles in affective
processing, some of which can be understood as relating to more general functions of these
regions outside of the emotional domain. Of the structures comprising the limbic system
hypothesis, the amygdala has been most consistently linked with emotional stimulus

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evaluation, a function originally attributed to the hypothalamus by previous theorists.

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10 Ohman A. Fear-relevance, autonomic conditioning, and phobias: A laboratory model. in
Sjoden PO, Bates S, Dockens WS (eds): Trends in Behavior Therapy. New York: Academic Press,
1979, pp 107-133.
11 Charney DS; Deutch A Y, & Krystal JH, et al. Psychobiologic mechanisms of posttraumatic stress
disorder. Arch Gen Psychiatry 50:294-305, 1993.
12 Adolphs R; Tranel D; Damasio H & Damasio AR. Impaired recognition of emotion in facial
expressions following bilateral damage to the human amygdala. Nature 372:669-672, 1994.
13 Aggleton JP. The functional effects of amygdala lesions in humans: A comparison with findings
from monkeys, in Aggleton JP (ed): The Amygdala: Neurobiological Aspects of Emotion, Mem-
ory, and Mental Dysfunction. New York: Wiley-Liss, 1992, pp 485-504.
14 Halgren E. Emotional neurophysiology of the amygdala within the context of human cognition,
in Aggleton JP (ed): The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental
Dysfunction. New York: Wiley-Liss, 1992, pp 191-228.
15 Slotnick BM. Fear behavior and passive avoidance deficits in mice with amygdala lesions.
Physiol Behav 11:717-720, 1973.
16 Gaffan D. Amygdala and the memory of reward, in Aggleton JP (ed): The Amygdala:
Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. New York: Wiley-Liss,
1992, pp 471-484.
17 Everitt BJ & Robbins TW. Amygdala-ventral striatal interactions and reward-related processes, in
Aggleton JP (ed): The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental
Dysfunction. New York: Wiley- Liss, 1992, pp 401-430.
18 Gray JA. The Psychology of Fear and Stress. 2d ed. Cambridge, England: Cambridge University
Press, 1987
19 Rolls ET. A theory of emotion and consciousness, and its application to understanding the
neural basis of emotion,in Gazzaniga M (ed): The Cognitive Neurosciences. Cambridge, MA:
MIT Press, 1995, pp 1091-1106.
20 Damasio A; Tranel D & Damasio H. Somatic markers and the guidance of behavior: Theory and
preliminary testing, in Levin H, Eisenberg H, Benton A (eds): Frontal Lobe Function and
Dysfunction. New York: Oxford University Press, 1991, pp 217-229.