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Cognitive Neuroscience
Emotion
I. Expression and Recognition of Emotion
The communication of emotion is very important for human interactions.
We display emotions by our actions, and perceive it in others by the
interpretation of those actions.
The scientific study of human emotional expression and recognition
depends on the use of human subjects.
Our understanding of human emotion comes from:
a) behavioral studies in normal subjects
b) behavioral studies of patients with brain lesions
c) imaging studies (PET & fMRI) of normals & brain-lesioned patients
What are the behavioral components by which we express and recognize
human emotion?
a) Facial expression
b) Hand gesture
c) Tone of voice
d) Word choice
To study human emotion, subjects are asked to recognize emotional
content in words or faces. They are asked to make judgments about
emotional content in sentences and scenes.
A. Facial Expression
The ability to perform and perceive facial expressions is a very important
part of human emotional communication.
Charles Darwin suggested that facial expressions are innate behavioral
responses.
Support comes from the similarity of these expressions in cultures
throughout the world. They are not culturally learned.
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Also, blind children display normal facial expressions à again suggesting
that they are not learned by observation.
Although facial expressions of emotion appear to be stereotyped behaviors,
they can be modified by social context. Sometimes cultures impose
restrictions on the expression of emotion.
A display rule is a cultural norm that modifies the expression of emotion in
different societal situations.
B. Neural Basis of Recognition
1. Studies of Hemispheric Difference
Some studies indicate that areas in the right hemisphere of the brain are
selectively involved in emotional comprehension.
a. Perceptual Studies in Normals
Tachistoscopic presentation of visual stimuli to one hemifield and dichotic
listening are used to compare the effects of presentation of material to the
left and right hemispheres.
The contralateral hemisphere to the side of presentation receives more
specific information than the ipsilateral side.
Subjects are found to respond more quickly and with greater accuracy (i.e.
fewer errors) in detecting emotional cues when stimuli are presented to the
right hemisphere than the left hemisphere.
b. Cortical Lesion Studies
i. Patients with right hemisphere cortical lesions are impaired in recognizing
the emotions expressed by facial expression and hand gesture. Ability to
recognize facial expression is independent of ability to recognize faces.
Adolphs study: right hemisphere lesions à selective recognition
impairment for negative emotions.
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ii. Patients with lesions in right temporal-parietal junction (rTPJ) cortex are
impaired in judging emotion expressed by tone of voice.
c. Imaging Studies
PET recording of rCBF while subjects assessed emotional content of verbal
input shows that the judgment of emotion from voice tone selectively
activates right prefrontal cortex.
2. Other Brain Structures
a. Amygdala
The amygdala is active when people perceive and recall emotional content.
It is also involved in emotional recognition:
i. people with bilateral amygdala lesions are impaired in the ability to
recognize facial expression of emotion. Impairment is particularly severe for
recognition of negative emotions such as fear.
ii. these people are also impaired in ability to assess threat from facial
expression, as compared to normals.
iii. normal subjects have elevated activity in the amygdala when viewing
facial expressions of fear.
b. Basal Ganglia
The basal ganglia appear to be specifically related to the ability to
recognize facial expressions of a particular emotion, disgust.
i. Impairment in the ability to recognize facial expressions of disgust found
in patients with degeneration (Huntingon’s disease) or malfunction
(obsessive-compulsive disorder) of basal ganglia.
ii. Increased activity in basal ganglia in neuroimaging of subjects viewing
facial expression of disgust.
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C. Neural Basis of Expression
1. Cortical Control of Facial Expression
As noted earlier, the facial expression of emotion is largely innate and
stereotyped.
Evidence suggests that these expressions involve different systems than
those involved in voluntary control of facial muscles:
a. Duchenne’s muscle (orbicularis oculi) contracts during a genuine smile,
but not a contrived smile.
b. Volitional facial paresis: partial paralysis of the facial musculature under
voluntary control, but activity of same muscles is normal in expression of
genuine emotions. Damage to primary motor cortex or its efferent
pathways.
c. Emotional facial paresis: voluntary control of facial musculature is
normal, but facial expression of emotion is impaired. Damage to insular
cortex or its efferent pathways.
2. Hemispheric Differences
As with recognition, facial expression of emotion has a stronger right
hemisphere component.
a. Chimerical face studies: stronger emotional content expressed by left
half of face than right.
b. Wada test studies: reduced emotional expression (i.e. less intense
emotions described) when right hemisphere put to sleep as compared to
baseline.
c. Stroke patients: right-hemisphere lesions impair ability to accurately
express emotion (facially & by tone of voice).
Also, patients with right-hemisphere damage show less concern for
disabilities than those with left-hemisphere damage.
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II. Theories of Emotion Generation
A. James-Lange Theory
William James and Carl Lange each proposed similar theories to explain
emotional experience.
It involves a three-step process:
1. Emotion-producing situations initially produce somatic physiological
responses, e.g. autonomic physiological changes, behavioral responses.
2. The brain receives sensory input from the viscera and muscles resulting
from the peripheral activations.
3. Interpretation of this secondary sensory input leads to the feeling
(experience) of emotion in higher brain regions, including the cerebral
cortex.
James-Lange theory thus implies that people cannot feel an emotion
without first having a bodily (somatic) response.
B. Cannon-Bard Theory
Cannon and Bard were Harvard physiologists who opposed the JamesLange theory on 5 major grounds:
1) total separation of viscera from the CNS does not eliminate emotional
behavior.
2) the same visceral responses occur in very different emotional states –
the sympathetic n.s. functions as a single unit, and somatic physiological
responses to emotion-producing situations are thus not distinct enough to
distinguish among different emotions.
3) the viscera are relatively insensitive to external stimulation.
4) somatic physiological processes are too slow to be the origin of different
emotions.
5) artificial production of emotion-related visceral changes does not actually
cause emotional experience.
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Cannon and Bard thus objected to the James-Lange theory because of its
postulate that the brain’s emotional response is secondary to the peripheral
response. Instead, they proposed that emotion involves simultaneous but
independent activity of the peripheral nervous system and the brain.
According to Cannon-Bard theory, the sympathetic n.s. coordinates the
body’s reaction to the situation, and the brain simultaneously generates
emotional feeling. Accordingly, emotional feeling does not need to follow
visceral input to the brain, and should be intact when that visceral input is
removed.
C. Appraisal Theory
In the various forms of appraisal theory, emotional processing depends on
the interaction between the properties of a stimulus and the interpretation
of those properties. For example, emotion may be a response to the
evaluation by the brain of the benefits and harms represented by an
external object. Thus, a cognitive appraisal, not necessarily conscious,
precedes the somatic physiological response and feeling.
D. Singer-Schachter Theory
This theory (sometimes called James-Lange-Schachter theory) is a blend
of James-Lange and appraisal theories.
Singer & Schachter proposed that cognitive appraisal of emotion follows
visceral input to the brain, and that this appraisal is required before an
emotion is experienced.
Evidence that visceral input to the brain is necessary for the experience of
emotion comes from the study of paraplegic (spinal-cord-injury) patients
(although this evidence is now considered controversial). It is claimed that
these patients continue to express (learned) emotional responses, but with
reduced emotional feeling. The subjective intensity of emotion experienced
by these patients is reported to correspond to the level of the lesion: i.e.,
the higher the transection, the less emotion is experienced. This finding is
explained by the hypothesis that the lower the transection, the greater the
loss of visceral input to the brain, and hence the lower the emotional
feeling.
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Schachter and Singer administered adrenaline to volunteers, creating an
ambiguous sense of arousal. These subjects would interpret the visceral
changes produced by the drug according to the context in which they were
put – e.g., they would say that they were experiencing feelings of fear if put
in a context of fear, or say that their feelings were drug induced if told that
they had received adrenaline.
E. Constructivist Theory
There are various forms of constructivist theory. They all suggest that
emotion emerges from cognition, as guided by culture and language.
The constructivist theory of Barrett holds that emotions are concepts that
are constructed by humans as we make meaning from sensory input
coming from the internal environment (body) and external environment.
First, a concept is constructed of primal bodily changes called core affect.
Then, this core affect is categorized according to language-based emotion
categories.
F. Evolutionary Psychology Theory
This approach proposes that emotions involve the (evolved) coordination of
physiological changes, behavioral tendencies, cognitive appraisals, and
emotional feelings. They are all orchestrated to produce adaptive
(successful) behavior.
G. LeDoux Theory
According to LeDoux, two neural emotion systems operate in parallel. The
first system generates emotional responses; the second generates the
feelings of emotion. The first is a fast system that is hardwired by evolution
to increase the likelihood of survival. The second is a slow system of
learned conscious responses.
III. The Amygdala & Implicit Emotion
In both humans and other species, the amygdala plays a critical role in
implicit emotion, as demonstrated by fear processing.
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LeDoux is a prominent cognitive neuroscientist who has studied fear
processing in the amygdala. Fear processing depends on the amygdala,
and the amygdala plays a major role in the processing of all emotions.
A. Kluver-Bucy Syndrome
In 1937, Kluver & Bucy reported on bilateral temporal lobe destruction in
monkeys that produced a dramatic behavioral syndrome:
a) wild animals became tame
b) flattening of emotions
c) oral tendencies -- put all kinds of encountered objects in mouth
d) became hypersexual -- great increase in sexual behavior & inappropriate
mounting
It is now known that these results come from destruction of temporal pole &
amygdala in particular.
B. Anatomy of the Amygdala
The amygdala is composed of numerous nuclei that are reciprocally
connected to the hypothalamus. Thus, the amygdala is in a position to
exert control over the hypothalamus, and over the many somatic responses
that the latter controls.
The amygdala is also connected with:
1) the nucleus acumbens -- part of the basal ganglia involved in reward
2) the orbitofrontal cortex
3 nuclei of the amygdala are most important for emotion:
(1) lateral nucleus (LA)
(2) basal nucleus (B)
(3) central nucleus (CE)
The LA projects to the B and the CE. The CE is the principal output nucleus
of the fear system. The CE projects to many areas of forebrain,
hypothalamus and brainstem that control:
(1) behavioral fear responses
(2) endocrine fear responses
(3) autonomic fear responses
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Damage to the CE interferes with the expression of all fear CRs. Thus,
the CE orchestrates the collection of hard-wired responses that underlie
defensive behavior.
IV. The Emotion of Fear
The study of fear conditioning in rodents has been very important for
revealing the neurobiology of emotion.
The study of fear conditioning has focused on three aspects of fear:
(1) how the brain learns to fear an object or situation
(2) how learned fears can guide the acquisition of behaviors that allow
avoidance of danger
(3) how fear can strengthen the memory formation of significant life
events
A. Learning to Fear
Pavlovian fear conditioning as a model system
Pavlovian fear conditioning of a rat involves exposing the animal to a
neutral stimulus, such as a tone (called the Conditioned Stimulus – CS) in
conjunction with an aversive stimulus, such as a brief electric shock (called
the Unconditioned Stimulus – US).
After as few as one CS-US pairing, the animal begins to elicit a range of
conditioned responses (CRs) to the CS and to the context in which
conditioning occurs.
In rats, the CR includes:
(1) immobility
(2) autonomic responses (e.g. increased heart rate, blood pressure)
(3) endocrine responses (e.g. increased levels of circulating stress
hormones)
(4) potentiation of reflexes (e.g. increased acoustic startle response)
In short, with conditioning the CS elicits many of the same defensive
responses as the US.
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Basic circuits of fear conditioning
In auditory fear conditioning in the rat, CS information about the tone is
transmitted to the auditory thalamus (medial division of medial geniculate
nucleus, MGm & posterior intralaminar nucleus, PIN) and then to auditory
cortex (area TE1 à TE3). The auditory thalamus and cortex send fiber
projections to the lateral nucleus of the amygdala (LA), with glutamate as
the transmitter.
Auditory fear conditioning depends on the pathway from the auditory
thalamus to the amygdala, but not from the auditory cortex. However, the
auditory cortex is required when the animal must discriminate between
different auditory CSs for conditioning to occur.
The same cells in LA that receive inputs from MGm/PIN and TE3 also
respond to foot shock, and thus may integrate information about the tone
and shock during fear conditioning. Thus, the LA is important for fear
acquisition.
Synaptic plasticity and fear conditioning
The LA appears to be an essential locus of plasticity for fear conditioning
because:
a) single neurons in the LA have been identified where pathways
converge carrying CS and US information.
b) the response of these cells to a CS is greatly increased following fear
conditioning.
c) fear conditioning is mediated by an associative LTP-like NMDAbased process in the LA.
Evidence for associative LTP in the LA:
a) after artificial LTP induction (i.e. due to tetanic electrical stimulation),
the CS evokes an enhanced response in LA.
b) fear conditioning produces similar electrophysiological changes in LA
c) associative LTP and fear conditioning in LA are sensitive to the same
disruptive effects from noncontingent postsynaptic LA neuron
depolarization
d) fear conditioning is impaired by pharmacological blockade of NMDA
receptors in the amygdala
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Contextual fear conditioning
Animals can be trained to fear context (e.g. the physical environment) by
conditioning with foot shock. Conditioning to context may accompany
auditory fear conditioning or may occur on its own.
1. The amygdala appears to be critically involved in storing the memory of
contextual fear conditioning.
(a) Lesions of the amygdala that include both the LA and basal nucleus
(B) disrupt both acquisition and expression of contextual fear
conditioning.
(b) contextual fear conditioning is also impaired by infusion of an NMDA
receptor antagonist in the amygdala.
It is not yet known which nuclei of the amygdala are critical for the memory,
but there is some evidence that the LA and anterior basal nucleus are
involved. The CE must be intact for the expression of contextual fear.
2. The hippocampus also appears to play a role in contextual fear
conditioning since lesions of hippocampus disrupt contextual fear
conditioning.
However, it is disrupted only by lesions that occur shortly after conditioning.
There appears to be a period of consolidation that requires hippocampal
involvement. Presumably, the contextual information is consolidated in the
neocortex.
It is hypothesized that the hippocampus is involved in 2 ways:
(a) to first form a representation of the context in which the conditioning
will occur
(b) to then provide the amygdala with contextual information during CSUS training
Anatomy: the hippocampus projects to the basal nucleus of the amygdala.
Immediate shock is not sufficient to support contextual fear conditioning.
But, if the animal is exposed to the conditioning environment prior to
training, then contextual fear conditioning is possible following immediate
shock. This indicates that the contextual representation must already be
formed prior to the fear conditioning.
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Retrieval and reactivation of fear memories
Memory retrieval may make the retrieved material susceptible to disruption
in a manner similar to a newly formed memory.
Following active recall of a fear memory, there appears to be a period of reconsolidation that requires protein synthesis in the amygdala: infusion of a
protein synthesis inhibitor into the amygdala immediately after retrieval of
auditory fear memory impairs memory recall on subsequent tests.
Hippocampal-dependent contextual memories also appear to be sensitive
to disruption at the time of retrieval.
It appears that hippocampal-independent contextual memory must return to
the hippocampus during retrieval and undergo a protein synthesisdependent reconsolidation in order to be retained.
B. The Role of Fear in Danger Avoidance
In instrumental (operant) fear learning, the animal learns to detect
dangerous objects or situations, and also uses the learned information to
guide ongoing behavior to actually avoid danger. The amygdala appears to
play a role in instrumental fear conditioning, as it does in Pavlovian fear
conditioning.
The projection from the LA to the basal nucleus appears to be involved in
instrumental fear conditioning.
In an escape-from-fear task:
a) lesion of LA disrupted both the Pavlovian and the instrumental
components of the task
b) lesion of CE impaired only the Pavlovian component
c) lesion of B impaired only the instrumental component
The basal nucleus of the amygdala may guide fear-related instrumental
conditioning through its projections to the basal ganglia.
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C. Strengthening of Memory Formation by Fear
Remember the distinction between implicit and explicit learning, and that
Pavlovian fear conditioning is a form of implicit learning.
However, in real-world situations Pavlovian fear conditioning may most
often occur along with explicit learning.
Explicit memory formation is believed to depend on the medial temporal
lobe memory system, consisting of the hippocampus and related cortical
areas, e.g. parahippocampal cortex, entorhinal cortex, etc.
During fearful (or other emotion-laden) experience, one route by which the
amygdala can influence explicit memory formation is by its projections to
the hypothalamus.
The amygdala can drive the hypothalamic-pituitary-adrenal (HPA) axis.
1. The hypothalamus releases corticotrophin releasing factor (CRF) into
specialized blood vessels serving the anterior pituitary gland.
2. The anterior pituitary is stimulated to release a number of different
hormones into the general circulation. One of these is
adrenocorticotrophic hormone (ACTH).
3. ACTH acts on the adrenal cortex to release glucocorticoids
(including cortisol) into the general circulation.
4. Glucocorticoids can cross the blood-brain barrier, and modulate the
function of amygdala, hippocampus and/or neocortex.
5. In addition to affecting the hippocampus hormonally, the amygdala
sends direct axonal projections to it.
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In inhibitory avoidance learning:
1) immediate post-training blockade of glucocorticoid receptors in the
amygdala impairs memory acquisition.
2) facilitation of those receptors enhances memory acquisition.
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