Ch 10. Emotional Learning
and Memory
Sue Corkin
Monday, Dec 3, 2007
today’s road map
•
•
•
•
•
•
•
•
•
what is the Papez circuit?
what is the limbic system?
classical fear conditioning
two routes for emotional learning: cortical and
subcortical
the amygdala
relation between the emotional memory system and
the declarative memory system
two dimensions: valence and arousal
what cognitive processes underlie the recollective
memory enhancement for emotional information?
what neural processes underlie the recollective
memory enhancement for emotional information?
Papez circuit
Feelings
•
•
•
•
•
•
hippocampal
formation
mammillary
Sensory
bodies
Cortex
anterior
thalamus
cingulate
cortex
parahippoThalamus
campal gyrus
hippocampal
formation
Emotional
Stimulus
Cingulate
Cortex
Anterior
Thalamus
Hippocampus
Hypothalamus
Bodily Response
Papez, James W. (1937) A proposed mechanism of emotion. Arch Neurol
Psychiat, 38, 725.
limbic system
•
•
•
•
hippocampal formation
amygdala (McLean)
cingulate gyrus
thalamus and hypothalamus
Broca, Paul (1878) Anatomie comparée des circonvolutions cérébrales. Le
grand lobe limbique et la scissure limbique dans la série des mammifères.
Rev. d’Anthrop, ser 2, 1, 285.
MacLean, Paul D. (1952) Some psychiatric implications of physiological
studies on frontotemporal portion of limbic system (visceral brain).
Electroencephalogr Clin Neurophysiol, 4, 407.
Cingulate Cortex
Hypothalamus
Amygdala
Mamillary body
of the Thalamus
X hypothalamus
Image courtesy of the NIH.
classical fear conditioning
Images removed due to copyright restrictions.
left: rat hears a sound, which has little effect on BP or movement
center: rat hears same sound, coupled with foot shock; after
several pairings, BP rises and rat freezes when it hears the sound
right: rat has been fear conditioned; sound alone achieves the
same physiological changes as did sound and shock together
LeDoux, 1994
what are the cerebral roots
of fear learning?
• is auditory cortex
required for auditory
fear conditioning? no
• what about auditory
thalamus? yes
• what about the
auditory midbrain?
yes
• What about the
hippocampus? no
Images removed due to copyright restrictions.
Illustration of rat brain with areas highlighted: auditory cortex,
hippocampus, auditory thalamus, and amygdala.
LeDoux, 1994
brain lesions have been crucial in
pinpointing the sites that mediate
experiencing and learning about fear
Images removed due to copyright restrictions.
The auditory pathway in the rat brain consists of sound entering the ear and being
turned into an electrical signal that travels down the auditory nerve to the auditory
midbrain, to the auditory thalamus, and finally to the auditory cortex.
If a lesion is made in the auditory midbrain or auditory thalamus, fear conditioning is
disrupted. If the lesion is made in the auditory cortex, however, conditioning is not
disrupted. These findings imply that the fear conditioning pathway involves the
auditory midbrain and auditory thalamus, but not the auditory cortex. The pathway
may involve additional, unknown structures.
LeDoux, 1994
auditory cortex is not needed to
establish simple fear conditioning
Images removed due to copyright restrictions.
The auditory pathway in the rat brain consists of sound entering the ear and being
turned into an electrical signal that travels down the auditory nerve to the auditory
midbrain, to the auditory thalamus, and finally to the auditory cortex.
If a lesion is made in the auditory midbrain or auditory thalamus, fear conditioning is
disrupted. If the lesion is made in the auditory cortex, however, conditioning is not
disrupted. These findings imply that the fear conditioning pathway involves the
auditory midbrain and auditory thalamus, but not the auditory cortex. The pathway
may involve additional, unknown structures.
LeDoux, 1994
BUT it is needed to interpret stimuli
when they become more intricate
• one of two stimuli was paired with foot shock
• intact rabbits expressed fear responses only to the
sound that had been coupled with the shock
• after receiving auditory cortex lesions, however, they
responded to both tones
• that is, when auditory cortex was absent, and animals
had to rely solely on the thalamus and amygdala for
learning, the two stimuli were indistinguishable
• conclusion: projections to the amygdala from sensory
regions of the cortex (e.g., auditory cortex) are
important in processing the emotional significance of
complex stimuli
LeDoux, 1994
anatomy of emotion
• cells in some regions of the auditory thalamus
give rise to fibers that reach several subcortical
locations
• could these neural projections be the
connections through which the stimulus elicits
the response we identify with fear?
• researchers made lesions in each of the
subcortical regions with which these fibers
connect
• the damage had an effect in only one area:
LeDoux, 1994
the amygdala
certain parts of the
thalamus (top - light pink)
communicate with areas in
the amygdala (bottom - light
yellow) that process the
fear-causing sound stimuli
LeDoux, 1994
Images removed due to copyright restrictions.
structure of the amygdala
Cortex
Thalamus
Lateral
nucleus
Accessory
basal nucleus
Stimulus
Hippocampus
Basal
nucleus
Central
nucleus
Amygdala
Figure by MIT OpenCourseWare.
lateral nucleus: receives input from sensory regions of the brain and
transmits these signals to the basolateral, accessory basal, and central
nuclei
central nucleus: connects to the brain stem, bringing about the
LeDoux, 1994
physiological changes
Image removed due to copyright restrictions.
Illustration of the intrinsic connections in the lateral nucleus of the amygdala.
See figure in Pitkanen, A., and D.G. Amaral. "Organization of the Intrinsic Connections of the Monkey and
Amygdaloid Complex: Projections Originating in the Lateral Nucleus." J Comp Neurol 398 (1998): 431-458.
Pitkanen & Amaral, 1998
neurochemical markers in the amygdala
•
•
•
•
•
•
•
•
•
•
•
•
•
•
Glutamate
NMDA/AMPA
Glutamine
GAD/GABA
Parvalbumin
Calbindin
Aspartate
Histimine
Dopamine
Norepinephrine
Epinephrine
Serotonin
AChE
ChAT
•
•
•
•
•
•
•
•
•
•
•
•
•
•
•
Somatostatin
Vasopressin
CRF
NGF
Cholecystokinin
Neuropeptide Y
Neurphysin
Estrogen
Neurotensin
Substance P
VIP
Enkephalin
Dynorphin
Protein kinase C
Benzodiazepene receptors
Stefanacci, 2???
Connections of the Amygdaloid Complex
Striatum
Basal forebrain
Thalamus
Claustrum
Amygdala
Hypothalamus
Brainstem
Hippocampal
formation
Neocortex
Occipital
Temporal
Insular
Cingulate
Frontal
Figure by MIT OpenCourseWare.
Amaral
more evidence that the amygdala
supports emotional memory
¾cells in the amygdala fire
during encoding of
emotional information
Image removed due to copyright restrictions.
MRI image of a human brain, with the amygdala highlighted.
copyright protected material used with permission of
author and University of Iowa’s Virtual Hospital,
www.vh.org
¾the magnitude of this
activation correlates with
likelihood of later retrieving
emotional information
patients with amygdalar
damage show a blunted
memory enhancement
effect
two routes for emotional learning:
one cortical and one subcortical
Image removed due to copyright restrictions.
The cortical route for emotional learning involves input from the senses - for
example, a visual stimulus - that travels to the visual thalamus, to the visual cortex, to
the amygdala. The subcortical route bypasses the visual cortex, with the signal
travelling to the visual thalamus and then straight to the amygdala.
LeDoux, 1994
the amygdala is not
the only learning center
• the establishment of memories is a function of
an entire network
• what about the hippocampus?
– important when learning and remembering are
conscious events (i.e., declarative memory)
– removal of the hippocampus in rats has little effect
on fear conditioning, but this is not declarative
learning (i.e., independent of conscious awareness)
– emotional information may be stored within
declarative memory, but it is kept there as a cold
declarative fact
LeDoux, 1994
relation between the emotional
memory system and the
declarative memory system
• emotional and declarative memories are stored and retrieved in
parallel
• their activities are joined seamlessly in our conscious
experience
• but that does not mean that we have direct conscious access to
emotional memory
• it means that we have access to the consequences (i.e., the
way we behave and the way our bodies feel)
• emotion exerts a powerful influence on declarative memory
• the amygdala plays an essential role in modulating the storage
and strength of declarative memories
LeDoux, 1994
slaughter
rape
High (exciting
or agitating)
emotional items differ from neutral items
along 2 dimensions: valence (negative or
positive) & arousal (calming or exciting)
AROUSAL
Low
(negative)
Low (calming)
VALENCE
High
(positive)
Russell, 1980; Lang et al., 1993
Low (calming)
Low
(negative)
AROUSAL
VALENCE
High (exciting
or agitating)
some items differed from the neutral ones primarily
in valence, and others differed primarily in arousal
High
(positive)
Russell, 1980; Lang et al., 1993
Low
NEGATIVE
(negative)
Low (calming)
VALENCE
AROUSAL
TABOO
High (exciting
or agitating)
some items differed from the neutral ones primarily
in valence, and others differed primarily in arousal
High
(positive)
Russell, 1980; Lang et al., 1993
study
orgasm
misery
+
translate
test
remember
orgasm
+
know
translate
purchase
new
Corrected Recognition
participants are more likely to “Remember” valence
(negative) than neutral words, and even more likely
to “Remember” high-arousal (taboo) words
80
70
60
R
*
K
N=20 men, ages 19-33
*
50
40
30
20
10
0
Taboo
Negative
Neutral
Kensinger & Corkin, 2003, Memory & Cognition
what cognitive processes underlie
memory enhancement for
negative, emotional information?
¾ participants remember the negative words better than
the neutral words because negative emotion
Ïincreases the subjective richness of memories, and
Ïincreases the contextual details associated with those
memories
¾ memory enhancement is stronger for arousing (taboo)
words than for non-arousing valence (negative) words
what cognitive processes underlie the
recollective memory enhancement
for emotional information?
CONTROLLED
(self-initiated)
• intentional, conscious
• attention-demanding
AUTOMATIC
OR
• incidental, not conscious
• not attention-demanding
elaborative encoding benefits memory
¾does the word
rhyme with
“pet”?
¾would the
word fit in the
sentence “He
met a _____ on
the street.”
Craik & Lockhart, 1975
70
Percentage Recognized
¾is the word in
capital letters?
60
50
40
30
20
10
0
Letters
Rhyme
Sentence
¾ negative emotional information
could be remembered better
because of controlled,
self-initiated processing
what cognitive processes underlie the
recollective memory enhancement
for emotional information?
CONTROLLED
(self-initiated)
• intentional, conscious
• attention-demanding
AUTOMATIC
OR
• incidental, not conscious
• not attention-demanding
relatively automatic and/or
prioritized processing of emotion
Image removed due to copyright restrictions.
The cortical route for emotional learning involves input from the senses - for
example, a visual stimulus - that travels to the visual thalamus, to the visual cortex, to
the amygdala. The subcortical route bypasses the visual cortex, with the signal
travelling to the visual thalamus and then straight to the amygdala.
LeDoux, 1994
Low
NEGATIVE
(negative)
Low (calming)
VALENCE
AROUSAL
TABOO
High (exciting
or agitating)
are there separate cognitive
mechanisms for valence and arousal?
High
(positive)
Russell, 1980; Lang et al., 1993
what is the role of attention
at encoding?
NO
HARD
EASY
NO
HARD
neutral
EASY
negative
COTTAGE
+
CEMETARY
taboo
ORGASM
Sound 1
Sound 2
no secondary task: “remember”
taboo > negative > neutral
80
Corrected Recognition
70
*
60
R
K
*
50
40
30
20
10
TAB
NEG
NEU
TAB
VAL
NEU
TAB
VAL
NEU
0
No Second Task
Easy second task
Hard second task
easy secondary task: “remember”
taboo > valence = neutral
Corrected Recognition
80
70
*
60
R
*
K
*
50
40
30
20
10
TAB
NEG
NEU
TAB
NEG
NEU
TAB
VAL
NEU
0
No Second Task
Easy Second Task
Hard second task
hard secondary task: “Remember”
taboo > valence = neutral
80
Corrected Recognition
70
*
60
R
*
K
*
*
50
40
30
20
10
TAB
NEG
NEU
TAB
NEG
NEU
TAB
NEG
NEU
0
No Second Task
Easy Second Task Hard Second Task
what cognitive processes underlie the
recollective memory enhancement for
emotional information?
VALENCE WORDS
CONTROLLED
(self-initiated)
• intentional, conscious
• attention-demanding
AROUSING
WORDS
AUTOMATIC
OR
• incidental, not conscious
• not attention-demanding
what neural structures support the
processing of valence and arousing words
to enhance recollection?
Image removed due to copyright restrictions.
Illustration of a brain with the prefrontal cortex, amygdala, and
hippocampus each highlighted.
prefrontal
cortex
amygdala
hippocampus
AROUSING
High (exciting
or agitating)
are there separate brain mechanisms
for valence and arousal?
VALENCE
AROUSAL
Low
(negative)
Low (calming)
VALENCE
High
(positive)
Russell, 1980; Lang et al., 1993
what brain regions support
memory enhancement?
14 men , 14 women
3T head-only Allegra scanner
data analyzed using SPM99
Negative, arousing
RAPE
Negative, nonarousing
SORROW
+
Fixation
MURDER Negative, arousing
FORECAST Neutral
memory performance during scanning
Memory as a function of wordtype and memory strength
Corrected Recognition
90
Know
Remember
80
70
60
50
40
30
20
10
0
Negative
Arousing
Valence-Only
Neutral
Negative
Nonarousin
g Kensinger & Corkin, PNAS, 2004
are there two brain networks
for emotional memory?
–one for valence (how positive or
negative the information is) and
–one for arousal (how exciting or
calming the information is)
subsequent memory paradigm
Question:
What was the
pattern of brain
activity when
people encoded
words they later
remembered vs.
when they
encoded words
they later forgot?
Wagner & Davachi, 2001
subsequent memory effect for valence (negative)
and neutral words: activation in 2 areas
predicted successful encoding
L inferior
PFC (BA 47)
*
*
0.35
0.3
0.25
0.2
0.15
0.1
0.05
es_R
rem
*
0.4
Peak % Signal Change
Peak
% Signal Change
Peak % Signal Change
0.4
0
L anterior
hippocampus
es_F
for
Valence
en_R
rem
en_F
for
Neutral
*
0.35
0.3
0.25
0.2
0.15
0.1
0.05
0
SR
SF
rem
for
Valence
NR
NF
rem
for
Neutral
Courtesy of National Academy of Sciences, U. S. A. Used with permission. Source: Kensinger, Elizabeth A., and Suzanne Corkin. "Two Routes to Emotional
Memory: Distinct Neural Processes for Valence and Arousal." PNAS 101 (2004): 3310-3315. Copyright 2004 National Academy of Sciences, U.S.A.
no subsequent memory effect in
L inferior PFC for arousing words
0.35
*
0.3
Peak % Signal Change
L inferior PFC
(BA 47)
*
0.25
0.2
0.15
0.1
0.05
0
eh_r
eh_m
rem
for
Arousal
es_r
es_m
rem
for
Valence
en_r
rem
for
Neutral
en_m
Courtesy of National Academy of Sciences, U. S. A. Used with permission. Source: Kensinger, Elizabeth A., and Suzanne Corkin. "Two Routes to Emotional
Memory: Distinct Neural Processes for Valence and Arousal." PNAS 101 (2004): 3310-3315. Copyright 2004 National Academy of Sciences, U.S.A.
0.4
Peak % Signal Change
L amygdala
™subsequent
memory effect
for arousing
(taboo) words
0.35
0.3
0.25
0.2
0.15
0.1
0.05
0
AR
AF
rem
for
Arousal
L anterior
hippocampus
0.35
Peak % Signal Change
activation
in 2 areas
predicted
successful
encoding
*
SR
SF
rem
for
Valence
NR
NF
for
rem
Neutral
*
*
0.3
*
0.25
0.2
0.15
0.1
0.05
0
AR
AF
rem
for
Arousal
SR
SF
rem
for
Valence
NR
NF
for
rem
Neutral
Courtesy of National Academy of Sciences, U. S. A. Used with permission. Source: Kensinger, Elizabeth A., and Suzanne Corkin. "Two Routes to Emotional
Memory: Distinct Neural Processes for Valence and Arousal." PNAS 101 (2004): 3310-3315. Copyright 2004 National Academy of Sciences, U.S.A.
amount of activation in these regions was correlated
significantly, suggesting that the 2 areas
act cooperatively
L amygdala
1
r = .60
0.8
0.6
0.4
0.2
L anterior
hippocampus
0
-0.1
0
-0.2
0.1
0.2
0.3
0.4
0.5
Peak % Signal Change in Hippocampus
-0.4
Courtesy of National Academy of Sciences, U. S. A. Used with permission. Source: Kensinger, Elizabeth A., and Suzanne
Corkin. "Two Routes to Emotional Memory: Distinct Neural Processes for Valence and Arousal." PNAS 101 (2004):
3310-3315. Copyright 2004 National Academy of Sciences, U.S.A.
0.6
a left prefrontal-hippocampal network
supports the recollective enhancement
for valence (negative) words
as well as for neutral words
left hippocampus
left prefrontal cortex
these areas support controlled processing of information,
which results in successful encoding
Courtesy of National Academy of Sciences, U. S. A. Used with permission. Source: Kensinger, Elizabeth A., and Suzanne Corkin. "Two Routes to Emotional
Memory: Distinct Neural Processes for Valence and Arousal." PNAS 101 (2004): 3310-3315. Copyright 2004 National Academy of Sciences, U.S.A.
an amygdalar-hippocampal network
supports the recollective enhancement
for arousing (taboo) words
automatic orienting toward emotional stimuli
may benefit memory
Courtesy of National Academy of Sciences, U. S. A. Used with permission. Source: Kensinger, Elizabeth A., and Suzanne Corkin. "Two Routes to Emotional
Memory: Distinct Neural Processes for Valence and Arousal." PNAS 101 (2004): 3310-3315. Copyright 2004 National Academy of Sciences, U.S.A.
conclusions
¾items with valence or with arousal are more
vividly remembered than neutral items
¾this effect is greater for arousing words than for
valence words
Word Type
Emotional Memory
Enhancement Effect
Neutral
Valence
Arousal
remember
different cognitive processes
support the enhancement effects
¾valence (negative) words are enhanced by
additional, elaborative, encoding processes
¾arousing (taboo) words are enhanced
automatically
Word Type
Emotional Memory
Enhancement Effect
Neutral
Valence
Arousal
remember
⇑
controlled
⇑
automatic
different neural processes
support the enhancement effects
Word Type
Neutral
Images removed due to copyright
restrictions.
Images of human brains with the
relevant areas highlighted.
Emotional Memory
Enhancement Effect
L inferior PFC, L hippocampus
(supports controlled processing)
Valence
Arousal
L amygdala, L hippocampus
(supports automatic processing)
time for
questions &
2 student
presentations
Image removed due to copyright restrictions.
Photo of a very stressed-looking woman.