Abstract
Numerous studies support the notion that emotional arousal modulates the formation of long-term memories. The amygdala, a principal component of the emotional memory system, is involved in modulating memory storage in other brain areas according to the emotional content of an encountered event. According to the concept of emotional tagging, activation of the amygdala during emotionally arousing events “tags” the experience as important by strengthening synapses located on neurons that have just been activated in other brain regions, mainly the hippocampus.
In line with this hypothesis, research has shown that activation of the amygdala by behavioral manipulations (exposing the subject to emotional content) or by electric stimulation could transform weak memories into strong, long-lasting ones. Although many studies emphasize the enhancing effect of amygdala activation on memory consolidation, a more complex picture emerges when observing emotional arousal under different conditions. Memory consolidation may be enhanced or impaired by emotional arousal, depending on such factors as the intensity of the emotional event, one’s ability to cope with it, and the timing of the event. Taking these complexities into consideration advances our understanding of the neural mechanisms behind emotional tagging and can provide insight into the neurobiology of affective disorders.
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References
Adolphs R, Cahill L, Schul R, Babinsky R (1997) Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learn Mem 4(3):291–300
Akirav I, Richter-Levin G (1999a) Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J Neurosci 19(23):10530–10535
Akirav I, Richter-Levin G (1999b) Priming stimulation in the basolateral amygdala modulates synaptic plasticity in the rat dentate gyrus. Neurosci Lett 270(2):83–86
Akirav I, Richter-Levin G (2002) Mechanisms of amygdala modulation of hippocampal plasticity. J Neurosci 22(22):9912–9921
Akirav I, Richter-Levin G (2006) Factors that determine the non-linear amygdala influence on hippocampus-dependent memory. Dose Response 4(1):22–37
Akirav I, Sandi C, Richter-Levin G (2001) Differential activation of hippocampus and amygdala following spatial learning under stress. Eur J Neurosci 14(4):719–725
Almaguer-Melian W, Martinez-Marti L, Frey JU, Bergado JA (2003) The amygdala is part of the behavioural reinforcement system modulating long-term potentiation in rat hippocampus. Neuroscience 119(2):319–322
Armony JL, LeDoux JE (1997) How the brain processes emotional information. Ann N Y Acad Sci 821:259–270
Bergado JA, Frey S, Lopez J, Almaguer-Melian W, Frey JU (2007) Cholinergic afferents to the locus coeruleus and noradrenergic afferents to the medial septum mediate LTP-reinforcement in the dentate gyrus by stimulation of the amygdala. Neurobiol Learn Mem 88(3):331–341
Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31–39
Brioni JD, Nagahara AH, McGaugh JL (1989) Involvement of the amygdala GABAergic system in the modulation of memory storage. Brain Res 487(1):105–112
Cahill L, McGaugh JL (1990) Amygdaloid complex lesions differentially affect retention of tasks using appetitive and aversive reinforcement. Behav Neurosci 104(4):532–543
Cahill L, McGaugh JL (1995) A novel demonstration of enhanced memory associated with emotional arousal. Conscious Cogn 4(4):410–421
Cahill L, Prins B, Weber M, McGaugh JL (1994) Beta-adrenergic activation and memory for emotional events. Nature 371(6499):702–704
Cahill L, Babinsky R, Markowitsch HJ, McGaugh JL (1995) The amygdala and emotional memory. Nature 377(6547):295–296
Da Cunha C, Roozendaal B, Vazdarjanova A, McGaugh JL (1999) Microinfusions of flumazenil into the basolateral but not the central nucleus of the amygdala enhance memory consolidation in rats. Neurobiol Learn Mem 72(1):1–7
Diamond DM, Rose GM (1994) Stress impairs LTP and hippocampal-dependent memory. Ann N Y Acad Sci 746:411–414
Diamond DM, Campbell AM, Park CR, Woodson JC, Conrad CD, Bachstetter AD, Mervis RF (2006) Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis. Hippocampus 16(7):571–576
Diamond DM, Campbell AM, Park CR, Halonen J, Zoladz PR (2007) The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson law. Neural Plast 2007:60803
Dolcos F, LaBar KS, Cabeza R (2004) Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron 42(5):855–863
Ferry B, McGaugh JL (1999) Clenbuterol administration into the basolateral amygdala post-training enhances retention in an inhibitory avoidance task. Neurobiol Learn Mem 72(1):8–12
Ferry B, McGaugh JL (2000) Role of amygdala norepinephrine in mediating stress hormone regulation of memory storage. Acta Pharmacol Sin 21(6):481–493
Ferry B, Roozendaal B, McGaugh JL (1999a) Basolateral amygdala noradrenergic influences on memory storage are mediated by an interaction between beta- and alpha1-adrenoceptors. J Neurosci 19(12):5119–5123
Ferry B, Roozendaal B, McGaugh JL (1999b) Involvement of alpha1-adrenoceptors in the basolateral amygdala in modulation of memory storage. Eur J Pharmacol 372(1):9–16
Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385(6616):533–536
Frey U, Morris RG (1998a) Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21(5):181–188
Frey U, Morris RG (1998b) Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37(4–5):545–552
Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452(1–2):57–65
Frey S, Bergado-Rosado J, Seidenbecher T, Pape HC, Frey JU (2001) Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP. J Neurosci 21(10):3697–3703
Garcia R (2001) Stress, hippocampal plasticity, and spatial learning. Synapse 40(3):180–183
Gerges NZ, Stringer JL, Alkadhi KA (2001) Combination of hypothyroidism and stress abolishes early LTP in the CA1 but not dentate gyrus of hippocampus of adult rats. Brain Res 922(2):250–260
Hamann SB, Ely TD, Grafton ST, Kilts CD (1999) Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nat Neurosci 2(3):289–293
Hatfield T, McGaugh JL (1999) Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiol Learn Mem 71(2):232–239
Hess WR, Akert K (1955) Experimental data on role of hypothalamus in mechanism of emotional behavior. AMA Arch Neurol Psychiatry 73:127–129
Ikegaya Y, Saito H, Abe K (1994) Attenuated hippocampal long-term potentiation in basolateral amygdala-lesioned rats. Brain Res 656(1):157–164
Ikegaya Y, Saito H, Abe K (1995a) Amygdala N-methyl-D-aspartate receptors participate in the induction of long-term potentiation in the dentate gyrus in vivo. Neurosci Lett 192(3):193–196
Ikegaya Y, Saito H, Abe K (1995b) High-frequency stimulation of the basolateral amygdala facilitates the induction of long-term potentiation in the dentate gyrus in vivo. Neurosci Res 22(2):203–207
Ikegaya Y, Saito H, Abe K (1996) The basomedial and basolateral amygdaloid nuclei contribute to the induction of long-term potentiation in the dentate gyrus in vivo. Eur J Neurosci 8(9):1833–1839
Ikegaya Y, Nakanishi K, Saito H, Abe K (1997) Amygdala beta-noradrenergic influence on hippocampal long-term potentiation in vivo. Neuroreport 8(14):3143–3146
Introini-Collison IB, Nagahara AH, McGaugh JL (1989) Memory enhancement with intra-amygdala post-training naloxone is blocked by concurrent administration of propranolol. Brain Res 476(1):94–101
Introini-Collison IB, Miyazaki B, McGaugh JL (1991) Involvement of the amygdala in the memory-enhancing effects of clenbuterol. Psychopharmacology 104(4):541–544
Introini-Collison IB, Dalmaz C, McGaugh JL (1996) Amygdala beta-noradrenergic influences on memory storage involve cholinergic activation. Neurobiol Learn Mem 65(1):57–64
Izaki Y, Arita J (1996) Long-term potentiation in the rat hippocampal CA1 region is inhibited selectively at the acquisition stage of discriminatory avoidance learning. Brain Res 723(1–2):162–168
Joels M, Krugers HJ (2007) LTP after stress: up or down? Neural Plast 2007:93202
Kademian SM, Bignante AE, Lardone P, McEwen BS, Volosin M (2005) Biphasic effects of adrenal steroids on learned helplessness behavior induced by inescapable shock. Neuropsychopharmacology 30(1):58–66
Kavushansky A, Vouimba RM, Cohen H, Richter-Levin G (2006) Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress. Hippocampus 16(1):35–42
Kensinger EA, Schacter DL (2006) Amygdala activity is associated with the successful encoding of item, but not source, information for positive and negative stimuli. J Neurosci 26(9):2564–2570
Kilpatrick L, Cahill L (2003) Modulation of memory consolidation for olfactory learning by reversible inactivation of the basolateral amygdala. Behav Neurosci 117(1):184–188
Kim JJ, Lee HJ, Han JS, Packard MG (2001) Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci 21(14):5222–5228
Kluver H, Bucy PC (1939) Preliminary analysis of the temporal lobes in monkeys. Arch Neurol Psychiatr 42:979–1000
Kogan I, Richter-Levin G (2008) Activation pattern of the limbic system following spatial learning under stress. Eur J Neurosci 27(3):715–722
Korz V, Frey JU (2005) Bidirectional modulation of hippocampal long-term potentiation under stress and no-stress conditions in basolateral amygdala-lesioned and intact rats. J Neurosci 25(32):7393–7400
Krug M, Lossner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13(1):39–42
LeDoux JE (1993) Emotional memory systems in the brain. Behav Brain Res 58(1–2):69–79
LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184
LeDoux J (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23(4–5):727–738
Liang KC, Hon W, Davis M (1994) Pre- and posttraining infusion of N-methyl-D-aspartate receptor antagonists into the amygdala impair memory in an inhibitory avoidance task. Behav Neurosci 108(2):241–253
Maren S (1996) Synaptic transmission and plasticity in the amygdala. An emerging physiology of fear conditioning circuits. Mol Neurobiol 13(1):1–22
Markowitsch HJ, Staniloiu A (2011) Amygdala in action: relaying biological and social significance to autobiographical memory. Neuropsychologia 49(4):718–733
Maroun M, Richter-Levin G (2003) Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J Neurosci 23(11):4406–4409
Matthies H (1989) Neurobiological aspects of learning and memory. Annu Rev Psychol 40:381–404
McGaugh JL (2002) Memory consolidation and the amygdala: a systems perspective. Trends Neurosci 25(9):456
McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1–28
McGaugh JL, Cahill L (1997) Interaction of neuromodulatory systems in modulating memory storage. Behav Brain Res 83(1–2):31–38
McGaugh JL, Roozendaal B (2002) Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12(2):205–210
McGaugh JL, McIntyre CK, Power AE (2002) Amygdala modulation of memory consolidation: interaction with other brain systems. Neurobiol Learn Mem 78(3):539–552
McIntyre CK, Marriott LK, Gold PE (2003) Cooperation between memory systems: acetylcholine release in the amygdala correlates positively with performance on a hippocampus-dependent task. Behav Neurosci 117(2):320–326
Otani S, Abraham WC (1989) Inhibition of protein synthesis in the dentate gyrus, but not the entorhinal cortex, blocks maintenance of long-term potentiation in rats. Neurosci Lett 106(1–2):175–180
Packard MG, Cahill L, McGaugh JL (1994) Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc Natl Acad Sci USA 91(18):8477–8481
Papez JW (1937) A proposed mechanism of emotion. Arch Neurol Psychiatr 38:724–744
Pitkanen A, Pikkarainen M, Nurminen N, Ylinen A (2000) Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann N Y Acad Sci 911:369–391
Richter-Levin G, Akirav I (2003) Emotional tagging of memory formation—in the search for neural mechanisms. Brain Res Brain Res Rev 43(3):247–256
Ritchey M, Dolcos F, Cabeza R (2008) Role of amygdala connectivity in the persistence of emotional memories over time: an event-related FMRI investigation. Cereb Cortex 18(11):2494–2504
Rodriguez AJ, Czaplinski K, Condeelis JS, Singer RH (2008) Mechanisms and cellular roles of local protein synthesis in mammalian cells. Curr Opin Cell Biol 20(2):144–149
Roesler R, Roozendaal B, McGaugh JL (2002) Basolateral amygdala lesions block the memory-enhancing effect of 8-Br-cAMP infused into the entorhinal cortex of rats after training. Eur J Neurosci 15(5):905–910
Roozendaal B, McGaugh JL (1996) Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol Learn Mem 65(1):1–8
Roozendaal B, McGaugh JL (1997) Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur J Neurosci 9(1):76–83
Roozendaal B, Portillo-Marquez G, McGaugh JL (1996) Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behav Neurosci 110(5):1074–1083
Roozendaal B, Quirarte GL, McGaugh JL (1997) Stress-activated hormonal systems and the regulation of memory storage. Ann N Y Acad Sci 821:247–258
Roozendaal B, Sapolsky RM, McGaugh JL (1998) Basolateral amygdala lesions block the disruptive effects of long-term adrenalectomy on spatial memory. Neuroscience 84(2):453–465
Roozendaal B, Griffith QK, Buranday J, De Quervain DJ, McGaugh JL (2003) The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: dependence on the basolateral amygdala. Proc Natl Acad Sci USA 100(3):1328–1333
Roozendaal B, McReynolds JR, McGaugh JL (2004) The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J Neurosci 24(6):1385–1392
Sah P, Faber ES, Lopez De Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83(3):803–834
Salinas JA, Introini-Collison IB, Dalmaz C, McGaugh JL (1997) Posttraining intraamygdala infusions of oxotremorine and propranolol modulate storage of memory for reductions in reward magnitude. Neurobiol Learn Mem 68(1):51–59
Sandi C, Loscertales M, Guaza C (1997) Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur J Neurosci 9(4):637–642
Sandi C, Woodson JC, Haynes VF, Park CR, Touyarot K, Lopez-Fernandez MA, Venero C, Diamond DM (2005) Acute stress-induced impairment of spatial memory is associated with decreased expression of neural cell adhesion molecule in the hippocampus and prefrontal cortex. Biol Psychiatry 57(8):856–864
Sapolsky RM (2003) Stress and plasticity in the limbic system. Neurochem Res 28(11):1735–1742
Seidenbecher T, Balschun D, Reymann KG (1995) Drinking after water deprivation prolongs “unsaturated” LTP in the dentate gyrus of rats. Physiol Behav 57(5):1001–1004
Seidenbecher T, Reymann KG, Balschun D (1997) A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proc Natl Acad Sci USA 94(4):1494–1499
Shors TJ, Seib TB, Levine S, Thompson RF (1989) Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244(4901):224–226
Shors TJ, Foy MR, Levine S, Thompson RF (1990) Unpredictable and uncontrollable stress impairs neuronal plasticity in the rat hippocampus. Brain Res Bull 24(5):663–667
Strange BA, Dolan RJ (2004) Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. Proc Natl Acad Sci USA 101(31):11454–11458
Straube T, Korz V, Balschun D, Frey JU (2003a) Requirement of beta-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus. J Physiol 552(Pt 3):953–960
Straube T, Korz V, Frey JU (2003b) Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus. Neurosci Lett 344(1):5–8
Tsoory MM, Vouimba RM, Akirav I, Kavushansky A, Avital A, Richter-Levin G (2008) Amygdala modulation of memory-related processes in the hippocampus: potential relevance to PTSD. Prog Brain Res 167:35–51
Uzakov S, Frey JU, Korz V (2005) Reinforcement of rat hippocampal LTP by holeboard training. Learn Mem 12(2):165–171
van Stegeren AH (2009) Imaging stress effects on memory: a review of neuroimaging studies. Can J Psychiatr 54(1):16–27
van Stegeren AH, Goekoop R, Everaerd W, Scheltens P, Barkhof F, Kuijer JP, Rombouts SA (2005) Noradrenaline mediates amygdala activation in men and women during encoding of emotional material. NeuroImage 24(3):898–909
Vazdarjanova A, McGaugh JL (1999) Basolateral amygdala is involved in modulating consolidation of memory for classical fear conditioning. J Neurosci 19(15):6615–6622
Vouimba RM, Richter-Levin G (2005) Physiological dissociation in hippocampal subregions in response to amygdala stimulation. Cereb Cortex 15(11):1815–1821
Vouimba RM, Yaniv D, Diamond D, Richter-Levin G (2004) Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats. Eur J Neurosci 19(7):1887–1894
Vouimba RM, Yaniv D, Richter-Levin G (2007) Glucocorticoid receptors and beta-adrenoceptors in basolateral amygdala modulate synaptic plasticity in hippocampal dentate gyrus, but not in area CA1. Neuropharmacology 52(1):244–252
Yerkes RM, Dodson JD (1908) The relation of strength of stimulus to rapidity of habit-formation. J Comp Neurol Psychol 18:459–482
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Richter-Levin, G., Kehat, O., Anunu, R. (2024). Emotional Tagging and Long-Term Memory Formation. In: Sajikumar, S., Abel, T. (eds) Synaptic Tagging and Capture. Springer, Cham. https://doi.org/10.1007/978-3-031-54864-2_18
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