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.