Replay of conditioned stimuli during late REM and stage N2 sleep influences affective tone rather than emotional memory strength

Neurobiology of Learning and Memory

Volumn 122, Issue , 2015, Pages 142-151

  Rihm, Julia S ^a,b   Rasch, Björn ^c,d  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c UNIVERSITY OF FRIBOURG   (Switzerland)

^d Zurich Center for Interdisciplinary Sleep Research (ZiS)   (Switzerland)

Author keywords

Emotional memory; Memory; N2; Pavlovian conditioning; Rapid eye movement sleep; Sleep; Targeted memory reactivation

Indexed keywords

HYDROCORTISONE;

ADULT; AFFECT; ALERTNESS; AROUSAL; ARTICLE; CONDITIONING; CONTROLLED STUDY; ELECTRODERMAL RESPONSE; ELECTROENCEPHALOGRAM; EMOTION; EMOTIONAL MEMORY; FEMALE; HUMAN; HUMAN EXPERIMENT; MEMORY; MEMORY CONSOLIDATION; NORMAL HUMAN; ODOR; RECALL; REM SLEEP; RESPONSE TIME; SLEEP STAGE; SOUND; STAGE N2 SLEEP; ADOLESCENT; BRAIN; CONDITIONED REFLEX; ELECTROENCEPHALOGRAPHY; PHYSIOLOGY; SMELLING; YOUNG ADULT;

ADOLESCENT; ADULT; AFFECT; AROUSAL; BRAIN; CONDITIONING, CLASSICAL; ELECTROENCEPHALOGRAPHY; EMOTIONS; FEMALE; GALVANIC SKIN RESPONSE; HUMANS; MEMORY; MENTAL RECALL; ODORS; OLFACTORY PERCEPTION; SLEEP STAGES; SLEEP, REM; YOUNG ADULT;

EID: 84930088710     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2015.04.008     Document Type: Article

References (60)

1. Antony J.W., Gobel E.W., O'Hare J.K., Reber P.J., Paller K.A. Cued memory reactivation during sleep influences skill learning. Nature Neuroscience 2012, 10.1038/nn.3152.
2. Atienza M., Cantero J.L. Complex sound processing during human REM sleep by recovering information from long-term memory as revealed by the mismatch negativity (MMN). Brain Research 2001, 901:151-160. 10.1016/S0006-8993(01)02340-X.
3. Baran B., Pace-Schott E.F., Ericson C., Spencer R.M.C. Processing of emotional reactivity and emotional memory over sleep. The Journal of Neuroscience 2012, 32(3):1035-1042. 10.1523/JNEUROSCI.2532-11.2012.
4. Bastuji H., Perrin F., Garcia-Larrea L. Semantic analysis of auditory input during sleep: Studies with event related potentials. International Journal of Psychophysiology 2002, 46:243-255. 10.1016/S0167-8760(02)00116-2.
5. Bonnet M.H., Carley D., Carskadon M., Easton P., Guilleminault C., Harper R., et al. EEG arousals: Scoring rules and examples. Sleep 1992, 15:173-184.
6. Boucsein W., Fowles D.C., Grimnes S., Ben-Shakhar G., Roth W.T., Dawson M.E., et al. Publication recommendations for electrodermal measurements. Psychophysiology 2012, 49(8):1017-1034. 10.1111/j.1469-8986.2012.01384.x.
7. Bradley M.M., Lang P.J. The international affective digitized sounds affective ratings of sounds and instruction manual. Emotion 2007, 29-46.
8. Buysse D.J., Reynolds C.F., Monk T.H., Berman S.R., Kupfer D.J. The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research. Psychiatry Research 1989, 28(2):193-213. 10.1016/0165-1781(89)90047-4.
9. Cahill L., McGaugh J.L. Mechanisms of emotional arousal and lasting declarative memory. Trends in Neurosciences 1998, 10.1016/S0166-2236(97)01214-9.
10. Cairney S.A., Durrant S.J., Hulleman J., Lewis P.A. Targeted memory reactivation during slow wave sleep facilitates emotional memory consolidation. Sleep 2014, 37:701-707. 10.5665/sleep.3572.
11. Cordi M.J., Diekelmann S., Born J., Rasch B. No effect of odor-induced memory reactivation during REM sleep on declarative memory stability. Frontiers in Systems Neuroscience 2014, 8. 10.3389/fnsys.2014.00157.
12. Cordi M.J., Schlarb A.a., Rasch B. Deepening sleep by hypnotic suggestion. Sleep 2014, 37:1143-1152. 10.5665/sleep.3778.
13. Covington J.W., Geisler M.W., Polich J., Murphy C. Normal aging and odor intensity effects on the olfactory event-related potential. International Journal of Psychophysiology 1999, 32(3):205-214. 10.1016/S0167-8760(99)00012-4.
14. Datta S., O'Malley M.W. Fear extinction memory consolidation requires potentiation of pontine-wave activity during REM sleep. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2013, 33:4561-4569. 10.1523/JNEUROSCI.5525-12.2013.
15. Ditye T., Javadi A.H., Carbon C.-C., Walsh V. Sleep facilitates long-term face adaptation. Proceedings of the Royal Society B - Biological Sciences 2013, 280:20131698. 10.1098/rspb.2013.1698.
16. Dumay N., Gaskell M.G. Sleep-associated changes in the mental representation of spoken words: Research report. Psychological Science 2007, 18:35-39. 10.1111/j.1467-9280.2007.01845.x.
17. Ellenbogen J.M., Hu P.T., Payne J.D., Titone D., Walker M.P. Human relational memory requires time and sleep. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:7723-7728. 10.1073/pnas.0700094104.
18. Fanselow M.S., LeDoux J.E. Why we think plasticity underlying pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 1999, 10.1016/S0896-6273(00)80775-8.
19. Ferdenzi C., Roberts S.C., Schirmer A., Delplanque S., Cekic S., Porcherot C., et al. Variability of affective responses to odors: Culture, gender, and olfactory knowledge. Chemical Senses 2013, 38(2):175-186. 10.1093/chemse/bjs083.
20. Freud, S. (1900). The interpretation of dreams.
21. Greenberg R., Pearlman C., Schwartz W.R., Grossman H.Y. Memory, emotion, and REM sleep. Journal of Abnormal Psychology 1983, 92:378-381. 10.1037/0021-843X.92.3.378.
22. Groch S., Wilhelm I., Diekelmann S., Born J. The role of REM sleep in the processing of emotional memories: Evidence from behavior and event-related potentials. Neurobiology of Learning and Memory 2013, 99:1-9. 10.1016/j.nlm.2012.10.006.
23. Hars B., Hennevin E., Pasques P. Improvement of learning by cueing during postlearning paradoxical sleep. Behavioural Brain Research 1985, 18(3):241-250. 10.1016/0166-4328(85)90032-4.
24. Hauner K.K., Howard J.D., Zelano C., Gottfried J.A. Stimulus-specific enhancement of fear extinction during slow-wave sleep. Nature Neuroscience 2013, 16:1553-1555. 10.1038/nn.3527.
25. Hennevin E., Huetz C., Edeline J.M. Neural representations during sleep: From sensory processing to memory traces. Neurobiology of Learning and Memory 2007, 87:416-440. 10.1016/j.nlm.2006.10.006.
26. Hobson J.A., Pace-Schott E.F., Stickgold R. Dreaming and the brain: Toward a cognitive neuroscience of conscious states. The Behavioral and Brain Sciences 2000, 23:793-842. (discussion 904-1121). 10.1017/S0140525X00003976.
27. Hu P., Stylos-Allan M., Walker M.P. Sleep facilitates consolidation of emotional declarative memory. Psychological Science 2006, 17(10):891-898. 10.1111/j.1467-9280.2006.01799.x.
28. Humphreys L.G. The effect of random alternation of reinforcement on the acquisition and extinction of conditioned eyelid reactions. Journal of Experimental Psychology 1939, 25(2):141-158.
29. Iber, C., Ancoli-Israel, S., Chesson, A. L., & Quan, S. F. (2007). The AASM manual for the scoring of sleep and associated events: Rules, terminology and technical specifications. (American Academy of Sleep Medicine, Ed.).
30. Little J.T., Johnson D.N., Minichiello M., Weingartner H., Sunderland T. Combined nicotinic and muscarinic blockade in elderly normal volunteers: Cognitive, behavioral, and physiologic responses. Neuropsychopharmacology 1998, 19:60-69. 10.1016/S0893-133X(98)00002-5.
31. Lorig T.S. The application of electroencephalographic techniques to the study of human olfaction: A review and tutorial. International Journal of Psychophysiology 2000, 36(2):91-104. 10.1016/S0167-8760(99)00104-X.
32. Louie K., Wilson M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 2001, 29:145-156. 10.1016/S0896-6273(01)00186-6.
33. Lykken D.T., Rose R., Luther B., Maley M. Correcting psychophysiological measures for individual differences in range. Psychological Bulletin 1966, 66:481-484. 10.1037/h0023922.
34. Maho C., Bloch V. Responses of hippocampal cells can be conditioned during paradoxical sleep. Brain Research 1992, 581:115-122. 10.1016/0006-8993(92)90350-I.
35. Maquet P., Péters J., Aerts J., Delfiore G., Degueldre C., Luxen A., et al. Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature 1996, 383(6596):163-166. 10.1038/383163a0.
36. Maren S. Neurobiology of Pavlovian fear conditioning. Annual Review of Neuroscience 2001, 24:897-931. 10.1146/annurev.neuro.24.1.897.
37. McGaugh J.L. Make mild moments memorable: Add a little arousal. Trends in Cognitive Sciences 2006, 10.1016/j.tics.2006.06.001.
38. Menz M.M., Rihm J.S., Salari N., Born J., Kalisch R., Pape H.C., et al. The role of sleep and sleep deprivation in consolidating fear memories. NeuroImage 2013, 75:87-96. 10.1016/j.neuroimage.2013.03.001.
39. Nishida M., Pearsall J., Buckner R.L., Walker M.P. REM sleep, prefrontal theta, and the consolidation of human emotional memory. Cerebral Cortex 2009, 19(5):1158-1166. 10.1093/cercor/bhn155.
40. Pavlov I.P. Conditioned reflexes 1927, Oxford University Press.
41. Payne J.D., Chambers A.M., Kensinger E.A. Sleep promotes lasting changes in selective memory for emotional scenes. Frontiers in Integrative Neuroscience 2012, 6:108. 10.3389/fnint.2012.00108.
42. Payne J.D., Kensinger E.A. Sleep's role in the consolidation of emotional episodic memories. Current Directions in Psychological Science 2010, 19(5):290-295. 10.1177/0963721410383978.
43. Poe G.R., Nitz D.A., McNaughton B.L., Barnes C.A. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Research 2000, 855:176-180. 10.1016/S0006-8993(99)02310-0.
44. Pruessner J.C., Kirschbaum C., Meinlschmid G., Hellhammer D.H. Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 2003, 28:916-931. 10.1016/S0306-4530(02)00108-7.
45. Rasch B., Born J. About sleep's role in memory. Physiological Reviews 2013, 93(2):681-766. 10.1152/physrev.00032.2012.
46. Rasch B., Büchel C., Gais S., Born J. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 2007, 315(5817):1426-1429. 10.1126/science.1138581.
47. Rolls A., Makam M., Kroeger D., Colas D., de Lecea L., Heller H.C. Sleep to forget: Interference of fear memories during sleep. Molecular Psychiatry 2013, 18(11):1166-1170. 10.1038/mp.2013.121.
48. Rudoy J.D., Voss J.L., Westerberg C.E., Paller K.A. Strengthening individual memories by reactivating them during sleep. Science 2009, 326(5956):1079. 10.1126/science.1179013.
49. Skinner B. The behavior of organisms: An experimental analysis. The psychological record 1938, Appleton-Century-Crofts, New York.
50. Smith C. Sleep states and learning: A review of the animal literature. Neuroscience and Biobehavioral Reviews 1985, 10.1016/0149-7634(85)90042-9.
51. Smith C. Sleep states, memory processes and synaptic plasticity. Behavioural Brain Research 1996, 78:49-56. 10.1016/0166-4328(95)00218-9.
52. Smith C., Weeden K. Post training REMs coincident auditory stimulation enhances memory in humans. Psychiatric Journal of the University of Ottawa: Revue de Psychiatrie de l'Universite d'Ottawa 1990, 15:85-90.
53. Solomon P.R., Vander Schaaf E.R., Thompson R.F., Weisz D.J. Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behavioral Neuroscience 1986, 100:729-744. 10.1037/0735-7044.100.5.729.
54. Sterpenich V., Schmidt C., Albouy G., Matarazzo L., Vanhaudenhuyse A., Boveroux P., et al. Memory reactivation during rapid eye movement sleep promotes its generalization and integration in cortical stores. Sleep 2014, 37(6):1061-1075. 10.5665/sleep.3762.
55. Thuerauf N., Reulbach U., Lunkenheimer J., Lunkenheimer B., Spannenberger R., Gossler A., et al. Emotional reactivity to odors: Olfactory sensitivity and the span of emotional evaluation separate the genders. Neuroscience Letters 2009, 456(2):74-79. 10.1016/j.neulet.2009.03.096.
56. Tsuno N., Besset A., Ritchie K. Sleep and depression. The Journal of Clinical Psychiatry 2005, 66:1254-1269. 10.4088/JCP.v66n1008.
57. Van der Helm E., Yao J., Dutt S., Rao V., Saletin J.M., Walker M.P. REM sleep depotentiates amygdala activity to previous emotional experiences. Current Biology: CB 2011, 21(23):2029-2032. 10.1016/j.cub.2011.10.052.
58. Wagner U., Fischer S., Born J. Changes in emotional responses to aversive pictures across periods rich in slow-wave sleep versus rapid eye movement sleep. Psychosomatic Medicine 2002, 64(4):627-634.
59. Wagner U., Gais S., Born J. Emotional memory formation is enhanced across sleep intervals with high amounts of rapid eye movement sleep. Learning & Memory 2001, 8(2):112-119. 10.1101/lm.36801.
60. Walker M.P., van der Helm E. Overnight therapy? The role of sleep in emotional brain processing. Psychological Bulletin 2009, 135(5):731-748. 10.1037/a0016570.