Gade Emotions and limbic structures 1: Amygdala Anders Gade, Copenhagen University

2 Gade Emotions : ’prehistory’ & history ’Limbic system’ concept: Origins Amygdala: anatomy and presumed function Patient studies of fear and amygdala Neuroimaging studies Subliminal activation and emotional blindsight (Amygdala enhances attention and memory) Outline

Gade Charles Darwin, 1872 The expression of the emotions in man and animals

angerdisgustfearhappinesssadnesssurprise Six basic emotions - Ekman faces William James, 1890: ”Courser emotions” (grief, fear, rage, love) vs. ”subtler emotions”

Gade James-Lange theory William James Carl Lange The expression precedes the feeling: ”we feel sad because we cry” ”we feel sad because we cry”

Gade My theory, on the contrary, is that the bodily changes follow directly the perception of the exciting fact, and that our feeling of the same changes as they occur IS the emotion. JAMES-LANGE TEORIEN Our natural way of thinking about.. emotions is that the mental perception of some fact excites the mental affection called the emotion, and that this latter state of mind gives rise to the bodily expression.

Gade Common-sense says,we lose our fortune, are sorry and weep; we meet a bear, are frightened and run; we are insulted by a rival, are angry and strike. The hypothesis here to be defended says that this order of sequence is incorrect, that the one mental state is not immediately induced by the other, that the bodily manifestations must first be interposed between, and that the more rational statement is that we feel sorry because we cry, angry because we strike, afraid because we tremble, and not that we cry, strike, or tremble, because we are sorry, angry, or fearful, as the case may be. Without the bodily states following on the perception, the latter would be purely cognitive in form, pale, colorless, destitute of emotional warmth. We might then see the bear, and judge it best to run, receive the insult and deem it right to strike, but we should not actually feel afraid or angry Assaulting dinosaur Heartbeat Fear James, 1890, bd. II, pp James, 1890, bd. II, pp

Gade, For den populære Forestilling er Sagen meget simpel: Sindsbevægelserne ere Entiteter, Substanser, Kræfter, "Dæmoner", der indvirke på Mennesket og frembringe aandelige og legemlige Forandringer hos det: "En Sorg ramte mig"; "en Glæde mødte mig"; "Rædsel greb mig” o.s.v..... Jeg tvivler ikke om, at den Moder, der sørger over sit Jeg tvivler ikke om, at den Moder, der sørger over sit døde Barn, vil protestere, maaske endog forarges, naar man siger til hende, at hvad hun føler, er sit Legemes Træthed og Slaphed, sin blodfattige Huds Kulde, sin Hjernes Mangel paa Evne til at tænke klart og rask - Alt belyst af Erindringen om disse Fænomeners Aarsag. Men der er ingen Grund til at indigneres; thi hendes Følelse bliver lige stærk, dyb og ren, hvad enten den stammer fra den ene Kilde eller fra den anden. Men den kan ikke eksistere uden sine legemlige Attributter. Tag hos den Rædselsslagne de legemlige Symptomer bort, lad hans Puls slaa roligt, hans Blik være livligt, hans Farve sund, hans Tanker klare - hvad bliver der saa tilovers af hans skræk? (Lange, 1885, pp og 61-62) Carl Lange, 1885: Om sindsbevægelser: et psykofysiologisk studie

9 Gade 1937 Papez’ circuit Klüver-Bucy syndrome MacLean: The triune brain / Limbic system Bilateral removal of medial temporal lobes in monkey: * loss of fear * uninhibited sexuality * hyperorality * ”psychic blindness” Hippoc. ACC ACC

10 Gade Paul D. MacLean - Limbic system … an affective sense of conviction of what is real, true, and important.. MacLean, 1970, p. 346 #632

Gade Weiskrantz, 1956: amygdala Amaral et al., Neuropsychologia 2003, 41: Bilateral amygdala-lesion: Loss of fear (a: grape fruit; b: rubber snake)

12 Gade Amygdala:input Freese & Amaral (2009). Neuroanatomy of the primate amygdala ch. 1 in Whalen & Phelps (eds.) The human amygdala, Guilford

13 Gade Amygdala output Basal forebrain - attention Hypothalamus - autonomic arousal Thalamus Brain stem PAG – freezing SN etc - Ventral striatum - Value assignment Cortex

14 Gade Amygdala - 3 main subnuclei

15 Gade John B. Watson Watson & Rayner (1920). Conditioned emotional reactions. J.Exp.Psychol., 3, 1-14 Fear conditioning

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17 Gade LeDoux, 1996

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19 Mats Fredrikson

20 Gade Temporal lobe epilepsy - Amygdala and fear 20% experience fear as a seizure; some as the only symptom. symptom. ”Wow! Den var god. Prøv den, Rasmussen - pirk ved den vinding, hvor jeg holder fingeren” Stimulation of amygdala provokes fear Videoklip 12A

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22 GadeAmygdalectomy Young et al., 1995, Brain, 118: #2650d

23 Gade Fear and amygdala - Pt. SM - bilateral amygdala-lesion Fear and amygdala - Pt. SM - bilateral amygdala-lesion (Urbach-Wiethe disease) (Urbach-Wiethe disease) Amygdala Amygdala - calcified and therefore imaged like bone on CT

24 Gade Frygt og amygdala - Pt. SM: bilateral amygdala-læsion (Urbach-Wiethe sygdom) 6) Kan ikke tegne ’frygt’ i et ansigt 1) Kan genkende personers identitet 2) Kan ubesværet lære nye 3) Kan ikke genkende frygt 4) Vurderer overraskelse og vrede som mindre intenst som mindre intenst 5) Ser ikke emotionelle blandings- tilstande tilstande 7) Kan ikke frygtbetinges

25 Gade 2. Parametric relation *Morris et al., 1996 (PET; fearful faces 0-125%) *Morris et al., 1996 (PET; fearful faces 0-125%) Amygdala in neuroimaging: from localization to Mechanisms: PET & fMRI studies from Fast habituation *Breiter et al., 1996 (fMRI; happy and fearful faces) *Breiter et al., 1996 (fMRI; happy and fearful faces) 1. Amygdala is activated mainly by negative emotional stimuli * Irwin et al., 1996 (fMRI; IAPS-pictures) *Zald & Pardo, 1997 (PET; foul smell) *Lane et al., 1997 (PET; IAPS-pictures)

26 Gade 5. This activation correlates with autonomic measures *Furmark et al., 1997 (PET; fear conditioning; electrodermal) *Furmark et al., 1997 (PET; fear conditioning; electrodermal) *La Bar et al., 1998 (fMRI; fear conditioning; SCR) *La Bar et al., 1998 (fMRI; fear conditioning; SCR) *Morris et al., 1998 (PET; masked faces; SCR) 6. Masked (preconscious) fear og fear conditioning *Whalen et al., 1998 (fMRI; masked fearful faces) *Whalen et al., 1998 (fMRI; masked fearful faces) *Morris et al., 1998, 1999 (PET; inc. covariation) *Morris et al., 1998, 1999 (PET; inc. covariation) 4. Amygdala is activated by conditioned fear *Furmark et al., 1997 (PET; snake video / shock) *La Bar et al., 1998 (fMRI; innocent visual stimuli / shock) *Morris et al., 1998,1999 (PET; masked angry faces / noise) Amygdala in neuroimaging: from localization to Mechanisms: PET & fMRI studies from 1996

27 Gade Amygdala:input ”quick and dirty” route (thalamic)

28 Gade Masked fearful faces: Preconscious emotional stimuli activate the amygdala Whalen et al., 1998, J.Neurosci. 18: AG# a694d

29 Gade Masked faces: Preconscious emotional stimuli activate amygdala fMRI: alternating 28 sec. epochs of masked fearful faces, masked happy faces, og fixation. Each epoch 56 stimuli. 8 of 10 subjects did not ”see” emotional facial expressions. Whalen et al., 1998, J.Neurosci. 18: AG# a694d

30 Gade fMRI m. 28 sek. epoker med skiftevis maskeret frygt, maskeret glæde, og fiksation. Hver epoke 56 stimuli. 8 af 10 fpp. ”så” ikke emotionelle ansigtsudtryk. Whalen et al., 1998 Masked faces: Preconscious emotional stimuli activate amygdala

31 Gade Whalen et al., 1998 #a694D Contrast: Fear - happiness Masked faces: Preconscious emotional stimuli activate amygdala

32 Gade Whalen et al., 1998 Contrast:Happiness - fixation Masked faces: Preconscious emotional stimuli activate amygdala

33 Gade Whalen et al., 1998 Area blown up: Contrasts: Fear / happy vs. fixation Fear:Bothsegments ↑ CBF Happy: in SI – ↓ in amygdala Masked faces: Preconscious emotional stimuli activate amygdala

34 Gade Preconscious fear learning What is the route to right amygdala for masked stimuli? Four areas with positive covariation: Morris, Öhman & Dolan, 1999 Pulvinar(thalamus) + superior colliculus + left hippocampus and right inferior occipital Gyrus (modulation?)

Gade Pegna et al., 2005: ”Emotional blindsight” # a694h 52 year old physician. Infarcts in in both V1 and cortikal blindness Recognition of emotional facial expressions (and no other stimuli) better than chance fMRI

36 Gade Morris et al. (2001). Brain, 124: # a695c ”Emotional blindsight” Amygdala-activation and its route. Patient G.Y. Significant covariance in superior colliculus and pulvinar Superior colliculus PulvinarAmygdala … the alternative, unconscious visual pathway – especially for danger signals signals

37 Gade Is the preconscious route important? Does it influence conscious processes ?

38 Gade A well-described monosynaptic connection to visual areas. Basis for emotional bias of visual attention Vuilleumier et al. (2004) Nat. Neurosci., 7, #2653a Vuilleumier, 2009; ch. 10 in Whalen & Phelps, ”The human amygdala”

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40 Gade de Gelder et al. (2005). PNAS, 102: # a695d ”Emotional blindsight” Unconscious amygdala-activation – modulation of conscious processes Patient G.Y. blind in right visual field x ?

41 Gade de Gelder et al. (2005). PNAS, 102: # a695d Patient G.Y. blind in right visual field x Test: fixate the cross ”Emotional blindsight” Unconscious amygdala-activation – modulation of conscious processes

42 Gade de Gelder et al. (2005). PNAS, 102: # a695d Patient G.Y. blind in right visual field x ”Emotional blindsight” Unconscious amygdala-activation – modulation of conscious processes

43 Gade de Gelder et al. (2005). PNAS, 102: # a695d Patient G.Y. blind in right visual field Experiment 1. Explicit task: which emotion ? (left) incongruent congruent conscious unconscious conscious unconscious 52,0 %44,4 % 41,1 % 81,1 % (p < 0.025) Chimeric faces: Fear – Fear 77 %; others chance ”Emotional blindsight” Unconscious amygdala-activation – modulation of conscious processes

44 Gade de Gelder et al. (2005). PNAS, 102: # a695d Patient G.Y. blind in right visual field x Effect of fear congruence on activation Modulation of brain activity - beyond amygdala - in superior colliculus and fusiform cortex Experiment 3: emotional voices: Corresponding effect on faces in the blind field ”Emotional blindsight” Unconscious amygdala-activation – modulation of conscious processes

Gade. AG# A652F/691B Cahill et al., x 12 videoklip i 2 FDG-PET-sessioner (12 emotionelle; 12 neutrale) Antal huskede film efter 3 uger Områder med signifikant korrelation mellem rGMR og huskede film Korrelation mellem glukoseomsætning i hø. amygdala og antal huskede film

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