Abstract
Emotional experiences have a privileged place in our memories. As humans are constantly inundated with information, this adaptive process allows for the preservation of more important emotionally salient events, while allowing less important information to be forgotten. Although the experience of emotion itself releases a bevy of neurochemical and neurophysiological reactions that can benefit memory, recent research indicates that sleep plays a vital role in the preferential processing that leads to long-term consolidation of emotional information. Behavioral, neuroimaging, and neuropsychological evidence suggests that sleep benefits the long-term storage of emotional memories by increasing activation and connectivity among the same brain regions responsible for the initial encoding of emotional experience, and by facilitating the integration of the various elements of the experience into higher level cortical networks. This chapter will review the behavioral and neurobiological evidence supporting enhanced memory for emotionally salient information and the role that sleep plays in this preferential processing. We will conclude with questions that remain in this field, highlighting areas that may be fruitful for future sleep and memory researchers to explore.
Keywords
- Emotional memory
- Memory consolidation
- Sleep
- Amygdala
- Hippocampus
- REM sleep
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- 1.
Importantly, there we no performance differences between the 9 am and 9 pm 30 min delay groups, and thus they were collapsed.
- 2.
Interestingly, participants who achieved REM during their naps also showed the most significant enhancements toward happy face stimuli, perhaps indicating a valence-dependent system. Few other studies have been able to replicate this effect, however.
References
Ackermann S, Rasch B (2014) Differential effects of non-REM and REM sleep on memory consolidation? Curr Neurol Neurosci Rep 14(2):1–10
Adolphs R, Cahill L, Schul R, Babinsky R (1997) Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learn Mem 4:291–300
Adolphs R, Denburg NL, Tranel D (2001) The amygdala’s role in long-term declarative memory for gist and detail. Behav Neurosci 115(5):983
Adolphs R, Tranel D, Buchanan T (2005) Amygdala damage impairs emotional memory for gist but not details of complex stimuli. Nat Neurosci 8:512–518
Alger S, Chambers A, Payne JD (2014). A nap rich in slow wave sleep selectively preserves emotional scene components. Poster session presented at the meeting of the Associated Professional Sleep Societies, LLC, Minneapolis, MN
Baran B, Pace-Schott EF, Ericson C, Spencer RM (2012) Processing of emotional reactivity and emotional memory over sleep. J Neurosci 32(3):1035–1042
Bennion KA, Steinmetz KRM, Kensinger EA, Payne JD (2013) Sleep and cortisol interact to support memory consolidation. Cereb Cortex bht255
Bird CM, Burgess N (2008) The hippocampus and memory: insights from spatial processing. Nat Rev Neurosci 9(3):182–194
Born J, Gais S (2000) REM sleep deprivation: the wrong paradigm leading to wrong conclusions. Behav Brain Sci 23(06):912–913
Born J, Wilhelm I (2012) System consolidation of memory during sleep. Psychol Res 76(2):192–203
Braun AR, Balkin TJ, Wesenten NJ, Carson RE, Varga M, Baldwin P, Selbie S, Belenky G, Herscovitch P (1997) Regional cerebral blood flow throughout the sleep-wake cycle. An H2 (15) O PET study. Brain 120(7):1173–1197
Buchanan TW, Adolphs R (2002) The role of the human amygdala in emotional modulation of long-term declarative memory. Adv Conscious Res 44:9–34
Burgess N, Maguire EA, O’Keefe J (2002) The human hippocampus and spatial and episodic memory. Neuron 35(4):625–641
Cahill L, Babinsky R, Markowitsch HJ, McGaugh JL (1995) The amygdala and emotional memory. Nature 377:295–296
Cahill L, Haier RJ, Fallon J, Alkire MT, Tang C, Keator D, Wull J, Mcgaugh JL (1996) Amygdala activity at encoding correlated with long-term, free recall of emotional information. Proc Natl Acad Sci 93(15):8016–8021
Cahill L, McGaugh JL (1995) A novel demonstration of enhanced memory associated with emotional arousal. Conscious Cogn 4(4):410–421
Cairney SA, Durrant SJ, Power R, Lewis PA (2014) Complimentary roles of slow-wave sleep and rapid eye movement sleep in emotional memory consolidation. Cereb Cortex bht349
Carr M, Nielsen T (2015) Morning rapid eye movement sleep naps facilitate broad access to emotional semantic networks. Sleep 38(3):433–443
Carskadon MA, Dement WC (2000) Normal human sleep: an overview. Principles Pract Sleep Med 4:13–23
Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129(3):564–583
Corkin S (2002) What’s new with the amnesic patient HM? Nat Rev Neurosci 3(2):153–160
Cunningham TJ, Chambers AM, Payne JD (2014a) Prospection and emotional memory: how expectation affects emotional memory formation following sleep and wake. Front Psychol 5(862)
Cunningham TJ, Crowell CR, Alger SE, Kensinger EA, Villano MA, Mattingly SM, Payne JD (2014b) Psychophysiological arousal at encoding leads to reduced reactivity but enhanced emotional memory following sleep. Neurobiol Learn Mem 114:155–164
Cunningham TJ, Pardilla-Delgado E, Alger S, Payne J (2014c) The role of REM sleep in emotional memory and affective reactivity in humans. In: Saylor C (ed) REM sleep: characteristics, disorders and physiological effects. Nova Science Publishers, New York
Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11(2):114–126
Dolcos F, Iordan AD, Kragel J, Stokes J, Campbell R, McCarthy G, Cabeza R (2013) Neural correlates of opposing effects of emotional distraction on working memory and episodic memory: an event-related FMRI investigation. Front Psychol 4:293. doi:10.3389/fpsyg.2013.00293
Gais S, Born J (2004) Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc Natl Acad Sci U S A 101(7):2140–2144
Gilson M, Deliens G, Leproult R, Bodart A, Nonclercq A, Ercek R, Peigneux P (2015) REM-enriched naps are associated with memory consolidation for sad stories and enhance mood-related reactivity. Brain Sci 6(1):1
Greenberg R, Pearlman C, Schwartz WR, Grossman HY (1983) Memory, emotion, and REM sleep. J Abnorm Psychol 92(3):378
Greenberg R, Pillard R, Pearlman C (1972) The effect of dream (stage REM) deprivation on adaptation to stress. Psychosom Med 34(3):257–262
Grieser C, Greenberg R, Harrison RH (1972) The adaptive function of sleep: the differential effects of sleep and dreaming on recall. J Abnorm Psychol 80(3):280
Groch S, Wilhelm I, Diekelmann S, Born J (2013) The role of REM sleep in the processing of emotional memories: evidence from behavior and event-related potentials. Neurobiol Learn Mem 99:1–9
Groch S, Wilhelm I, Diekelmann S, Sayk F, Gais S, Born J (2011) Contribution of norepinephrine to emotional memory consolidation during sleep. Psychoneuroendocrinology 36(9):1342–1350
Groch S, Zinke K, Wilhelm I, Born J (2015) Dissociating the contributions of slow-wave sleep and rapid eye movement sleep to emotional item and source memory. Neurobiol Learn Mem 122:122–130
Gujar N, McDonald SA, Nishida M, Walker MP (2011) A role for REM sleep in recalibrating the sensitivity of the human brain to specific emotions. Cereb Cortex 21(1):115–123
Hamann S (2001) Cognitive and neural mechanisms of emotional memory. Trends Cogn Sci 5(9):394–400
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
Hasselmo ME (1999) Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3(9):351–359
Hasselmo ME, McGaughy J (2004) High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine. Acetylcholine Cereb Cortex 24:207
Henson RN, Hornberger M, Rugg MD (2005) Further dissociating the processes involved in recognition memory: an FMRI study. J Cogn Neurosci 17(7):1058–1073
Hu P, Stylos-Allan M, Walker MP (2006) Sleep facilitates consolidation of emotional declarative memory. Psychol Sci 17(10):891–898
Huijgen J, Samson S (2015) The hippocampus: a central node in a large-scale brain network for memory. Revue Neurologique 171(3):204–216
Jones MW, Wilson MA (2005) Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 15(7):867
Kensinger EA, Corkin S (2003) Memory enhancement for emotional words: are emotional words more vividly remembered than neutral words? Mem Cogn 31(8):1169–1180
Kensinger EA, Garoff-Eaton RJ, Schacter DL (2006) Memory for specific visual details can be enhanced by negative arousing content. J Mem Lang 54(1):99–112
Kleinsmith LJ, Kaplan S (1963) Paired-associate learning as a function of arousal and interpolated interval. J Exp Psychol 65(2):190
LaBar KS, Cabeza R (2006) Cognitive neuroscience of emotional memory. Nat Rev Neurosci 7(1):54–64
Lang PJ (1995) The emotion probe: studies of motivation and attention. Am Psychol 50(5):372
Lang PJ, Bradley MM, Cuthbert BN (1997) International affective picture system (IAPS): technical manual and affective ratings. NIMH Cent Study Emot Attention 39–58
Lang PJ, Greenwald MK, Bradley MM, Hamm AO (1993) Looking at pictures: Affective, facial, visceral, and behavioral reactions. Psychophysiology 30(3):261–273
Lara-Carrasco J, Nielsen TA, Solomonova E, Levrier K, Popova A (2009) Overnight emotional adaptation to negative stimuli is altered by REM sleep deprivation and is correlated with intervening dream emotions. J Sleep Res 18(2):178–187
Lena I, Parrot S, Deschaux O, Muffat-Joly S, Sauvinet V, Renaud BEEA, Gottesmann C (2005) Variations in extracellular levels of dopamine, noradrenaline, glutamate, and aspartate across the sleep–wake cycle in the medial prefrontal cortex and nucleus accumbens of freely moving rats. J Neurosci Res 81(6):891–899
Loftus EF, Loftus GR, Messo J (1987) Some facts about “weapon focus”. Law Hum Behav 11(1):55
Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29(1):145–156
Maloney KJ, Mainville L, Jones BE (2002) c-Fos expression in dopaminergic and GABAergic neurons of the ventral mesencephalic tegmentum after paradoxical sleep deprivation and recovery. Eur J Neurosci 15(4):774–778
Maquet P (1997) REM sleep and amygdala. Mol Psychiatry 2(3)
Maquet P, Péters JM, Aerts J, Delfiore G, Degueldre C, Luxen A, Franck G (1996) Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature 383(6596):163–166
Markowitsch HJ, Calabrese P, Würker M, Durwen HF, Kessler J, Babinsky R, Brechtelsbauer D, Heuser L, Gehlen W (1994) The amygdala’s contribution to memory-a study on two patients with Urbach-Wiethe disease. Neuroreport 5(11):1349–1352
Marrosu F, Portas C, Mascia MS, Casu MA, Fà M, Giagheddu M, Imperato A, Gessa GL (1995) Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats. Brain Res 671(2):329–332
McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1–28
Mehta MA, Hinton EC, Montgomery AJ, Bantick RA, Grasby PM (2005) Sulpiride and mnemonic function: effects of a dopamine D2 receptor antagonist on working memory, emotional memory and long-term memory in healthy volunteers. J Psychopharmacol 19(1):29–38
Mölle M, Yeshenko O, Marshall L, Sara SJ, Born J (2006) Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J Neurophysiol 96(1):62–70
Mueller EM, Pizzagalli DA (2015) One-year-old fear memories rapidly activate human fusiform gyrus. Soc Cogn Affect Neurosci nsv122
Nadel L, Moscovitch M (1997) Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 7(2):217–227
Nir Y, Tononi G (2010) Dreaming and the brain: from phenomenology to neurophysiology. Trends Cogn Sci 14(2):88–100
Nishida M, Pearsall J, Buckner RL, Walker MP (2009) REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cereb Cortex 19(5):1158–1166
Nofzinger EA, Mintun MA, Wiseman M, Kupfer DJ, Moore RY (1997) Forebrain activation in REM sleep: an FDG PET study. Brain Res 770(1):192–201
Nowicka A, Marchewka A, Jednoróg K, Tacikowski P, Brechmann A (2010) Forgetting of emotional information is hard: an fMRI study of directed forgetting. Cereb Cortex bhq117
Pace-Schott EF, Hobson JA (2002) The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat Rev Neurosci 3(8):591–605
Pace-Schott EF, Shepherd E, Spencer RM, Marcello M, Tucker M, Propper RE, Stickgold R (2011) Napping promotes inter-session habituation to emotional stimuli. Neurobiol Learn Mem 95(1):24–36
Paré D, Collins DR, Pelletier JG (2002) Amygdala oscillations and the consolidation of emotional memories. Trends Cogn Sci 6(7):306–314
Payne JD (2010) Memory consolidation, the diurnal rhythm of cortisol, and the nature of dreams: a new hypothesis. Int rev neurobiol 92:101–134
Payne JD, Chambers AM, Kensinger EA (2012) Sleep promotes lasting changes in selective memory for emotional scenes. Front Integr Neurosci 6(108):1–11
Payne JD, Kensinger EA (2010) Sleep’s role in the consolidation of emotional episodic memories. Curr Dir Psychol Sci 19(5):290–295
Payne JD, Kensinger EA (2011) Sleep leads to changes in the emotional memory trace: evidence from FMRI. J Cogn Neurosci 23(6):1285–1297
Payne JD, Kensinger EA, Wamsley EJ, Spreng RN, Alger SE, Gibler K, Stickgold R (2015) Napping and the selective consolidation of negative aspects of scenes. Emotion 15(2):176
Payne JD, Swanberg K, Stickgold R, Kensinger EA (2008) Sleep preferentially enhances memory for emotional components of scenes. Psychol Sci 19:781–788
Peigneux P, Laureys S, Fuchs S, Collette F, Perrin F, Reggers J, Phillips C, Degueldre C, Del Fiore G, Aerts J, Luxen A, Maquet P (2004) Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44(3):535–545
Phelps EA (2004) Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 14(2):198–202
Plihal W, Born J (1997) Effects of early and late nocturnal sleep on declarative and procedural memory. J Cogn Neurosci 9(4):534–547
Power AE (2004) Muscarinic cholinergic contribution to memory consolidation: with attention to involvement of the basolateral amygdala. Curr Med Chem 11(8):987–996
Prehn-Kristensen A, Göder R, Chirobeja S, Breßmann I, Ferstl R, Baving L (2009) Sleep in children enhances preferentially emotional declarative but not procedural memories. J Exp Child Psychol 104(1):132–139
Rasch B, Born J (2013) About sleep’s role in memory. Physiol Rev 93(2):681–766
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
Ritchey M, LaBar KS, Cabeza R (2011) Level of processing modulates the neural correlates of emotional memory formation. J Cogn Neurosci 23(4):757–771
Rosales-Lagarde A, Armony JL, del Río-Portilla Y, Trejo-Martínez D, Conde R, Corsi-Cabrera M (2012) Enhanced emotional reactivity after selective REM sleep deprivation in humans: an fMRI study. Mem Motivational/Emotional Processes 182
Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20(1):11
Schacter DL, Addis DR (2007a) Constructive memory: the ghosts of past and future. Nature 445(7123):27–27
Schacter DL, Addis DR (2007b) The cognitive neuroscience of constructive memory: remembering the past and imagining the future. Philos Trans R Soc Lond B Biol Sci 362(1481):773–786
Siapas AG, Wilson MA (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 21:1123–1128
Sirota A, Csicsvari J, Buhl D, Buzsáki G (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci U S A 100(4):2065–2069
Smith CT, Aubrey JB, Peters KR (2004) Different roles for REM and stage 2 sleep in motor learning: a proposed model. Psychol Belg 44:81–104
Sotres-Bayon F, Bush DE, LeDoux JE (2004) Emotional perseveration: an update on prefrontal-amygdala interactions in fear extinction. Learn Mem 11(5):525–535
Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99(2):195
Steriade M, Nuñez A, Amzica F (1993) Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13(8):3266–3283
Sterpenich V, Albouy G, Boly M, Vandewalle G, Darsaud A, Balteau E, Vu TTD, Desseilles M, D’Argembeau A, Gais S, Rauchs G, Schabus CD, Luxen A, Collette F, Maquet P (2007) Sleep-related hippocampo-cortical interplay during emotional memory recollection. PLoS Biol 5(11):e282
Sterpenich V, Albouy G, Darsaud A, Schmidt C, Vandewalle G, Vu TTD, Desseilles M, Phillips C, Degueldre C, Balteau E, Collette F, Luxen A, Maquet P (2009) Sleep promotes the neural reorganization of remote emotional memory. J Neurosci 29(16):5143–5152
Strange BA, Dolan RJ (2006) Anterior medial temporal lobe in human cognition: memory for fear and the unexpected. Cogn Neuropsychiatry 11(3):198–218
Stickgold R, Walker MP (2013) Sleep-dependent memory triage: evolving generalization through selective processing. Nat Neurosci 16(2):139–145
Takashima A, Petersson KM, Rutters F, Tendolkar I, Jensen O, Zwarts MJ, McNaughton B, Fernandez G (2006) Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. Proc Natl Acad Sci U S A 103(3):756–761
Talmi D (2013) Enhanced emotional memory cognitive and neural mechanisms. Curr Dir Psychol Sci 22(6):430–436
Wagner U, Fischer S, Born J (2002) Changes in emotional responses to aversive pictures across periods rich in slow-wave sleep versus rapid eye movement sleep. Psychosom Med 64(4):627–634
Wagner U, Gais S, Born J (2001) Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learn Mem 8(2):112–119
Wagner U, Hallschmid M, Rasch B, Born J (2006) Brief sleep after learning keeps emotional memories alive for years. Biol Psychiatry 60(7):788–790
Walker MP (2009) Sleep, memory and emotion. Prog Brain Res 185:49–68
Walker MP, Brakefield T, Morgan A, Hobson JA, Stickgold R (2002) Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron 35(1):205–211
Walker MP, Stickgold R (2010) Overnight alchemy: sleep-dependent memory evolution. Nat Rev Neurosci 11(3):218–218
Walker MP, van Der Helm E (2009) Overnight therapy? The role of sleep in emotional brain processing. Psychol Bull 135(5):731
van der Helm E, Walker MP (2012) Sleep and affective brain regulation. Soc Pers Psychol Compass 6(11):773–791
van der Helm E, Yao J, Dutt S, Rao V, Saletin JM, Walker MP (2011) REM sleep depotentiates amygdala activity to previous emotional experiences. Curr Biol 21(23):2029–2032
Vazquez J, Baghdoyan HA (2001) Basal forebrain acetylcholine release during REM sleep is significantly greater than during waking. Am J Physiol-Regul Integr Comp Physiol 280(2):R598–R601
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Cunningham, T.J., Payne, J.D. (2017). Emotional Memory Consolidation During Sleep. In: Axmacher, N., Rasch, B. (eds) Cognitive Neuroscience of Memory Consolidation. Studies in Neuroscience, Psychology and Behavioral Economics. Springer, Cham. https://doi.org/10.1007/978-3-319-45066-7_9
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