Sleep-dependent memory consolidation and its implications for psychiatry

Goerke, Monique; Müller, Notger G.; Cohrs, Stefan

doi:10.1007/s00702-015-1476-3

Psychiatry and Preclinical Psychiatric Studies - Review Article
Published: 30 October 2015

Sleep-dependent memory consolidation and its implications for psychiatry

Monique Goerke^1,2,
Notger G. Müller¹ &
Stefan Cohrs²

Journal of Neural Transmission volume 124, pages 163–178 (2017)Cite this article

1623 Accesses
13 Citations
1 Altmetric
Metrics details

Abstract

Both sleep disturbance and memory impairment are very common in psychiatric disorders. Since sleep has been shown to play a role in the process of transferring newly acquired information into long-term memory, i.e., consolidation, it is important to highlight this link in the context of psychiatric disorders. Along these lines, after providing a brief overview of healthy human sleep, current neurobiological models on sleep-dependent memory consolidation and resultant opportunities to manipulate the memory consolidation process, recent findings on sleep disturbances and sleep-dependent memory consolidation in patients with insomnia, major depression, schizophrenia, and post-traumatic stress disorder are systematically reviewed. Furthermore, possible underlying neuropathologies and their implications on therapeutic strategies are discussed. This review aims at sensitizing the reader for recognizing sleep disturbances as a potential contributor to cognitive deficits in several disorders, a fact which is often overlooked up to date.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Notes

The Role of REM sleep in memory consolidation, particularly in the consolidation of complex skills, has been challenged rather to depend on the paradigm used [see(Ackermann and Rasch (2014)] or on the learning potential of the subject (Smith et al. 2004).

References

Ackermann S, Rasch B (2014) Differential effects of non-REM and REM sleep on memory consolidation? Curr Neurol Neurosci Rep 14(2):430. doi:10.1007/s11910-013-0430-8
PubMed Article Google Scholar
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Publishing, Arlington
Book Google Scholar
Amos T, Stein DJ, Ipser JC (2014) Pharmacological interventions for preventing post-traumatic stress disorder (PTSD). Cochrane Database Syst Rev 7:CD006239. doi:10.1002/14651858.CD006239.pub2
Google Scholar
Antony JW, Gobel EW, O’Hare JK, Reber PJ, Paller KA (2012) Cued memory reactivation during sleep influences skill learning. Nat Neurosci 15(8):1114–1116. doi:10.1038/nn.3152
CAS PubMed PubMed Central Article Google Scholar
Armitage R, Hoffmann RF, Rush AJ (1999) Biological rhythm disturbance in depression: temporal coherence of ultradian sleep EEG rhythms. Psychol Med 29(6):1435–1448
CAS PubMed Article Google Scholar
Backhaus J, Junghanns K, Born J, Hohaus K, Faasch F, Hohagen F (2006) Impaired declarative memory consolidation during sleep in patients with primary insomnia: influence of sleep architecture and nocturnal cortisol release. Biol Psychiatry 60(12):1324–1330. doi:10.1016/j.biopsych.2006.03.051
CAS PubMed Article Google Scholar
Baglioni C, Regen W, Teghen A, Spiegelhalder K, Feige B, Nissen C, Riemann D (2013) Sleep changes in the disorder of insomnia: a meta-analysis of polysomnographic studies. Sleep Med Rev 18(3):195–213. doi:10.1016/j.smrv.2013.04.001
Article Google Scholar
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. doi:10.1523/JNEUROSCI.2532-11.2012
CAS PubMed PubMed Central Article Google Scholar
Bastien CH, St-Jean G, Turcotte I, Morin CM, Lavallee M, Carrier J (2009) Sleep spindles in chronic psychophysiological insomnia. J Psychosom Res 66(1):59–65. doi:10.1016/j.jpsychores.2008.05.013
PubMed Article Google Scholar
Besset A, Villemin E, Tafti M, Billiard M (1998) Homeostatic process and sleep spindles in patients with sleep-maintenance insomnia: effect of partial (21 h) sleep deprivation. Electroencephalogr Clin Neurophysiol 107(2):122–132. doi:10.1016/S0013-4694(98)00048-0
CAS PubMed Article Google Scholar
Binder S, Rawohl J, Born J, Marshall L (2014) Transcranial slow oscillation stimulation during NREM sleep enhances acquisition of the radial maze task and modulates cortical network activity in rats. Front Behav Neurosci 7:220. doi:10.3389/fnbeh.2013.00220
PubMed PubMed Central Article Google Scholar
Bonnet MH, Arand DL (2010) Hyperarousal and insomnia: state of the science. Sleep Med Rev 14(1):9–15. doi:10.1016/j.smrv.2009.05.002
PubMed Article Google Scholar
Boutros NN, Mucci A, Diwadkar V, Tandon R (2014) Negative symptoms in schizophrenia. Clin Schizophr Relat Psychoses 8(1):28–35B. doi:10.3371/CSRP.BOMU.012513
PubMed Article Google Scholar
Breslau N, Roth T, Burduvali E, Kapke A, Schultz L, Roehrs T (2004) Sleep in lifetime posttraumatic stress disorder: a community-based polysomnographic study. Arch Gen Psychiatry 61(5):508–516. doi:10.1001/archpsyc.61.5.508
PubMed Article Google Scholar
Brunet A, Poundja J, Tremblay J, Bui E, Thomas E, Orr SP, Azzoug A, Birmes P, Pitman RK (2011) Trauma reactivation under the influence of propranolol decreases posttraumatic stress symptoms and disorder: 3 open-label trials. J Clin Psychopharmacol 31(4):547–550. doi:10.1097/JCP.0b013e318222f360
PubMed Article Google Scholar
Buchegger J, Meier-Koll A (1988) Motor learning and ultradian sleep cycle: an electroencephalographic study of trampoliners. Percept Mot Skills 67(2):635–645. doi:10.2466/pms.1988.67.2.635
CAS PubMed Article Google Scholar
Buchegger J, Fritsch R, Meier-Koll A, Riehle H (1991) Does trampolining and anaerobic physical fitness affect sleep? Percept Mot Skills 73(1):243–252. doi:10.2466/pms.1991.73.1.243
CAS PubMed Article Google Scholar
Cairney SA, Durrant SJ, Hulleman J, Lewis PA (2014a) Targeted memory reactivation during slow wave sleep facilitates emotional memory consolidation. Sleep 37(4):701–707. doi:10.5665/sleep.3572
PubMed PubMed Central Google Scholar
Cairney SA, Durrant SJ, Power R, Lewis PA (2014b) Complementary roles of slow-wave sleep and rapid eye movement sleep in emotional memory consolidation. Cereb Cortex. doi:10.1093/cercor/bht349
PubMed Google Scholar
Caldwell DF, Domino EF (1967) Electroencephalographic and eye movement patterns during sleep in chronic schizophrenic patients. Electroencephalogr Clin Neurophysiol 22(5):414–420
CAS PubMed Article Google Scholar
Cellini N, de Zambotti M, Covassin N, Sarlo M, Stegagno L (2014) Impaired off-line motor skills consolidation in young primary insomniacs. Neurobiol Learn Mem 114:141–147. doi:10.1016/j.nlm.2014.06.006
PubMed Article Google Scholar
Chouinard S, Poulin J, Stip E, Godbout R (2004) Sleep in untreated patients with schizophrenia: a meta-analysis. Schizophr Bull 30(4):957–967
PubMed Article Google Scholar
Cohen DJ, Begley A, Alman JJ, Cashmere DJ, Pietrone RN, Seres RJ, Germain A (2013) Quantitative electroencephalography during rapid eye movement (REM) and non-REM sleep in combat-exposed veterans with and without post-traumatic stress disorder. J Sleep Res 22(1):76–82. doi:10.1111/j.1365-2869.2012.01040.x
PubMed Article Google Scholar
Cohrs S (2008) Sleep disturbances in patients with schizophrenia: impact and effect of antipsychotics. CNS Drugs 22(11):939–962. doi:10.2165/00023210-200822110-00004
CAS PubMed Article Google Scholar
Cohrs S, Rodenbeck A, Hornyak M, Kunz D (2008) Restless legs syndrome, periodic limb movements, and psychopharmacology. Nervenarzt 79(11):1263–1272. doi:10.1007/s00115-008-2575-2
CAS PubMed Article Google Scholar
Cowdin N, Kobayashi I, Mellman TA (2014) Theta frequency activity during rapid eye movement (REM) sleep is greater in people with resilience versus PTSD. Exp Brain Res 232(5):1479–1485. doi:10.1007/s00221-014-3857-5
PubMed PubMed Central Article Google Scholar
De Gennaro L, Ferrara M (2003) Sleep spindles: an overview. Sleep Med Rev 7(5):423–440. doi:10.1053/smrv.2002.0252
PubMed Article Google Scholar
De Jong J, Wauben P, Huijbrechts I, Oolders H, Haffmans J (2010) Doxazosin treatment for posttraumatic stress disorder. J Clin Psychopharmacol 30(1):84–85. doi:10.1097/JCP.0b013e3181c827ae
PubMed Article Google Scholar
de Maertelaer V, Hoffman G, Lemaire M, Mendlewicz J (1987) Sleep spindle activity changes in patients with affective disorders. Sleep 10(5):443–451
PubMed Google Scholar
Deliens G, Peigneux P (2014) One night of sleep is insufficient to achieve sleep-to-forget emotional decontextualisation processes. Cognit Emot 28(4):698–706. doi:10.1080/02699931.2013.844105
Article Google Scholar
Deliens G, Gilson M, Schmitz R, Peigneux P (2013a) Sleep unbinds memories from their emotional context. Cortex 49(8):2221–2228. doi:10.1016/j.cortex.2012.11.014
PubMed Article Google Scholar
Deliens G, Neu D, Peigneux P (2013b) Rapid eye movement sleep does not seem to unbind memories from their emotional context. J Sleep Res 22(6):656–662. doi:10.1111/jsr.12065
PubMed Article Google Scholar
Deliens G, Gilson M, Peigneux P (2014) Sleep and the processing of emotions. Exp Brain Res 232(5):1403–1414. doi:10.1007/s00221-014-3832-1
PubMed Article Google Scholar
Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11(2):114–126. doi:10.1038/nrn2762
CAS PubMed Google Scholar
Dresler M, Genzel L, Kluge M, Schüssler P, Weber F, Rosenhagen M, Steiger A (2010a) Off-line memory consolidation impairments in multiple sclerosis patients receiving high-dose corticosteroid treatment mirror consolidation impairments in depression. Psychoneuroendocrinology 35(8):1194–1202. doi:10.1016/j.psyneuen.2010.02.005
CAS PubMed Article Google Scholar
Dresler M, Kluge M, Genzel L, Schüssler P, Steiger A (2010b) Impaired off-line memory consolidation in depression. Eur Neuropsychopharmacol 20(8):553–561. doi:10.1016/j.euroneuro.2010.02.002
CAS PubMed Article Google Scholar
Dresler M, Kluge M, Pawlowski M, Schüssler P, Steiger A, Genzel L (2011) A double dissociation of memory impairments in major depression. J Psychiatr Res 45(12):1593–1599. doi:10.1016/j.jpsychires.2011.07.015
PubMed Article Google Scholar
Ebdlahad S, Nofzinger EA, James JA, Buysse DJ, Price JC, Germain A (2013) Comparing neural correlates of REM sleep in posttraumatic stress disorder and depression: a neuroimaging study. Psychiatry Res 214(3):422–428. doi:10.1016/j.pscychresns.2013.09.007
PubMed Article Google Scholar
Ebrahim IO, Shapiro CM, Williams AJ, Fenwick PB (2013) Alcohol and sleep I: effects on normal sleep. Alcohol Clin Exp Res 37(4):539–549. doi:10.1111/acer.12006
CAS PubMed Article Google Scholar
Eggert T, Dorn H, Sauter C, Nitsche MA, Bajbouj M, Danker-Hopfe H (2013) No effects of slow oscillatory transcranial direct current stimulation (tDCS) on sleep-dependent memory consolidation in healthy elderly subjects. Brain Stimul 6(6):938–945. doi:10.1016/j.brs.2013.05.006
PubMed Article Google Scholar
Feige B, Baglioni C, Spiegelhalder K, Hirscher V, Nissen C, Riemann D (2013) The microstructure of sleep in primary insomnia: an overview and extension. Int J Psychophysiol 89(2):171–180. doi:10.1016/j.ijpsycho.2013.04.002
PubMed Article Google Scholar
Feld GB, Wilhelm I, Ma Y, Groch S, Binkofski F, Molle M, Born J (2013) Slow wave sleep induced by GABA agonist tiagabine fails to benefit memory consolidation. Sleep 36(9):1317–1326. doi:10.5665/sleep.2954
PubMed PubMed Central Google Scholar
Ferrarelli F, Huber R, Peterson MJ, Massimini M, Murphy M, Riedner BA, Watson A, Bria P, Tononi G (2007) Reduced sleep spindle activity in schizophrenia patients. Am J Psychiatry 164(3):483–492. doi:10.1176/appi.ajp.164.3.483
PubMed Article Google Scholar
Ferrarelli F, Peterson MJ, Sarasso S, Riedner BA, Murphy MJ, Benca RM, Bria P, Kalin NH, Tononi G (2010) Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. Am J Psychiatry 167(11):1339–1348. doi:10.1176/appi.ajp.2010.09121731
PubMed PubMed Central Article Google Scholar
Gais S, Born J (2004) Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation. Proc Natl Acad Sci USA 101(7):2140–2144. doi:10.1073/pnas.0305404101
CAS PubMed PubMed Central Article Google Scholar
Gais S, Rasch B, Dahmen JC, Sara S, Born J (2011) The memory function of noradrenergic activity in non-REM sleep. J Cognit Neurosci. doi:10.1162/jocn.2011.21622
Google Scholar
Gehrman P, Seelig AD, Jacobson IG, Boyko EJ, Hooper TI, Gackstetter GD, Ulmer CS, Smith TC (2013) Predeployment sleep duration and insomnia symptoms as risk factors for new-onset mental health disorders following military deployment. Sleep 36(7):1009–1018. doi:10.5665/sleep.2798
PubMed PubMed Central Google Scholar
Genzel L, Dresler M, Cornu M, Jager E, Konrad B, Adamczyk M, Friess E, Steiger A, Czisch M, Goya-Maldonado R (2014a) Medial prefrontal-hippocampal connectivity and motor memory consolidation in depression and schizophrenia. Biol Psychiatry. doi:10.1016/j.biopsych.2014.06.004
PubMed Google Scholar
Genzel L, Kroes MC, Dresler M, Battaglia FP (2014b) Light sleep versus slow wave sleep in memory consolidation: a question of global versus local processes? Trends Neurosci 37(1):10–19. doi:10.1016/j.tins.2013.10.002
CAS PubMed Article Google Scholar
Genzel L, Spoormaker VI, Konrad BN, Dresler M (2015) The role of rapid eye movement sleep for amygdala-related memory processing. Neurobiol Learn Mem 122:110–121. doi:10.1016/j.nlm.2015.01.008
CAS PubMed Article Google Scholar
Germain A (2013) Sleep disturbances as the hallmark of PTSD: where are we now? Am J Psychiatry 170(4):372–382. doi:10.1176/appi.ajp.2012.12040432
PubMed PubMed Central Article Google Scholar
Germain A, Hall M, Katherine Shear M, Nofzinger EA, Buysse DJ (2006) Ecological study of sleep disruption in PTSD: a pilot study. Ann N Y Acad Sci 1071:438–441. doi:10.1196/annals.1364.038
PubMed Article Google Scholar
Germain A, James J, Insana S, Herringa RJ, Mammen O, Price J, Nofzinger E (2013) A window into the invisible wound of war: functional neuroimaging of REM sleep in returning combat veterans with PTSD. Psychiatry Res 211(2):176–179. doi:10.1016/j.pscychresns.2012.05.007
PubMed Article Google Scholar
Göder R, Boigs M, Braun S, Friege L, Fritzer G, Aldenhoff JB, Hinze-Selch D (2004) Impairment of visuospatial memory is associated with decreased slow wave sleep in schizophrenia. J Psychiatr Res 38(6):591–599. doi:10.1016/j.jpsychires.2004.04.005
PubMed Article Google Scholar
Göder R, Aldenhoff JB, Boigs M, Braun S, Koch J, Fritzer G (2006) Delta power in sleep in relation to neuropsychological performance in healthy subjects and schizophrenia patients. J Neuropsychiatry Clin Neurosci 18(4):529–535. doi:10.1176/appi.neuropsych.18.4.529
PubMed Article Google Scholar
Göder R, Fritzer G, Gottwald B, Lippmann B, Seeck-Hirschner M, Serafin I, Aldenhoff JB (2008) Effects of olanzapine on slow wave sleep, sleep spindles and sleep-related memory consolidation in schizophrenia. Pharmacopsychiatry 41(3):92–99. doi:10.1055/s-2007-1004592
PubMed Article CAS Google Scholar
Göder R, Seeck-Hirschner M, Stingele K, Huchzermeier C, Kropp C, Palaschewski M, Aldenhoff J, Koch J (2011) Sleep and cognition at baseline and the effects of REM sleep diminution after 1 week of antidepressive treatment in patients with depression. J Sleep Res 20:544–551. doi:10.1111/j.1365-2869.2011.00914.x
PubMed Article Google Scholar
Göder R, Baier PC, Beith B, Baecker C, Seeck-Hirschner M, Junghanns K, Marshall L (2013) Effects of transcranial direct current stimulation during sleep on memory performance in patients with schizophrenia. Schizophr Res 144(1–3):153–154. doi:10.1016/j.schres.2012.12.014
PubMed Article Google Scholar
Goerke M, Cohrs S, Rodenbeck A, Grittner U, Sommer W, Kunz D (2012) Declarative memory consolidation during the first night in a sleep lab: the role of REM sleep and cortisol. Psychoneuroendocrinology. doi:10.1016/j.psyneuen.2012.10.019
PubMed Google Scholar
Goerke M, Rodenbeck A, Cohrs S, Kunz D (2013) The influence of the tricyclic antidepressant amitriptyline on periodic limb movements during sleep. Pharmacopsychiatry. doi:10.1055/s-0032-1331702
PubMed Google Scholar
Goerke M, Cohrs S, Rodenbeck A, Kunz D (2014) Differential effect of an anticholinergic antidepressant on sleep-dependent memory consolidation. Sleep 37(5):977–985. doi:10.5665/sleep.3674
PubMed PubMed Central Google Scholar
Goldstein AN, Walker MP (2014) The role of sleep in emotional brain function. Annu Rev Clin Psychol 10:679–708. doi:10.1146/annurev-clinpsy-032813-153716
PubMed PubMed Central Article Google Scholar
Griessenberger H, Heib DP, Lechinger J, Luketina N, Petzka M, Moeckel T, Hoedlmoser K, Schabus M (2013) Susceptibility to declarative memory interference is pronounced in primary insomnia. PLoS One 8(2):e57394. doi:10.1371/journal.pone.0057394
CAS PubMed PubMed Central Article Google Scholar
Gupta MA (2013) Review of somatic symptoms in post-traumatic stress disorder. Int Rev Psychiatry 25(1):86–99. doi:10.3109/09540261.2012.736367
PubMed Article Google Scholar
Hasler BP, Insana SP, James JA, Germain A (2013) Evening-type military veterans report worse lifetime posttraumatic stress symptoms and greater brainstem activity across wakefulness and REM sleep. Biol Psychol 94(2):255–262. doi:10.1016/j.biopsycho.2013.06.007
PubMed PubMed Central Article Google Scholar
Hauner KK, Howard JD, Zelano C, Gottfried JA (2013) Stimulus-specific enhancement of fear extinction during slow-wave sleep. Nat Neurosci 16(11):1553–1555. doi:10.1038/nn.3527
CAS PubMed PubMed Central Article Google Scholar
Hiatt JF, Floyd TC, Katz PH, Feinberg I (1985) Further evidence of abnormal non-rapid-eye-movement sleep in schizophrenia. Arch Gen Psychiatry 42(8):797–802
CAS PubMed Article Google Scholar
Hoedlmoser K, Pecherstorfer T, Gruber G, Anderer P, Doppelmayr M, Klimesch W, Schabus M (2008) Instrumental conditioning of human sensorimotor rhythm (12-15 Hz) and its impact on sleep as well as declarative learning. Sleep 31(10):1401–1408
PubMed PubMed Central Google Scholar
Hoffmann R, Hendrickse W, Rush AJ, Armitage R (2000) Slow-wave activity during non-REM sleep in men with schizophrenia and major depressive disorders. Psychiatry Res 95(3):215–225. doi:10.1016/S0165-1781(00)00181-5
CAS PubMed Article Google Scholar
Hoge EA, Worthington JJ, Nagurney JT, Chang Y, Kay EB, Feterowski CM, Katzman AR, Goetz JM, Rosasco ML, Lasko NB, Zusman RM, Pollack MH, Orr SP, Pitman RK (2012) Effect of acute posttrauma propranolol on PTSD outcome and physiological responses during script-driven imagery. CNS Neurosci Ther 18(1):21–27. doi:10.1111/j.1755-5949.2010.00227.x
CAS PubMed Article Google Scholar
Hornung OP, Regen F, Danker-Hopfe H, Schredl M, Heuser I (2007) The relationship between REM sleep and memory consolidation in old age and effects of cholinergic medication. Biol Psychiatry 61(6):750–757. doi:10.1016/j.biopsych.2006.08.034
CAS PubMed Article Google Scholar
Huang L, Zhou J, Li Z, Lei F, Tang X (2012) Sleep perception and the multiple sleep latency test in patients with primary insomnia. J Sleep Res 21(6):684–692. doi:10.1111/j.1365-2869.2012.01028.x
PubMed Article Google Scholar
Hudson SM, Whiteside TE, Lorenz RA, Wargo KA (2012) Prazosin for the treatment of nightmares related to posttraumatic stress disorder: a review of the literature. Prim Care Companion CNS Disord. doi:10.4088/PCC.11r01222
PubMed PubMed Central Google Scholar
Iber C, Ancoli-Israel S, Chesson AL, Quan SF (2007) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications. American Academy of Sleep Medicine, Westchester
Google Scholar
Jacobsen RB, Ulrich D, Huguenard JR (2001) GABA(B) and NMDA receptors contribute to spindle-like oscillations in rat thalamus in vitro. J Neurophysiol 86(3):1365–1375
CAS PubMed Google Scholar
Kaestner EJ, Wixted JT, Mednick SC (2013) Pharmacologically increasing sleep spindles enhances recognition for negative and high-arousal memories. J Cognit Neurosci 25(10):1597–1610. doi:10.1162/jocn_a_00433
Article Google Scholar
Karni A, Tanne D, Rubenstein BS, Askenasy JJ, Sagi D (1994) Dependence on REM sleep of overnight improvement of a perceptual skill. Science 265(5172):679–682
CAS PubMed Article Google Scholar
Keshavan MS, Reynolds CF 3rd, Miewald MJ, Montrose DM, Sweeney JA, Vasko RC Jr, Kupfer DJ (1998) Delta sleep deficits in schizophrenia: evidence from automated analyses of sleep data. Arch Gen Psychiatry 55(5):443–448
CAS PubMed Article Google Scholar
Kessler RC, Sonnega A, Bromet E, Hughes M, Nelson CB (1995) Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry 52(12):1048–1060
CAS PubMed Article Google Scholar
Kobayashi I, Boarts JM, Delahanty DL (2007) Polysomnographically measured sleep abnormalities in PTSD: a meta-analytic review. Psychophysiology 44(4):660–669. doi:10.1111/j.1469-8986.2007.537.x
PubMed Article Google Scholar
Krystal AD, Goforth HW, Roth T (2008) Effects of antipsychotic medications on sleep in schizophrenia. Int Clin Psychopharmacol 23(3):150–160. doi:10.1097/YIC.0b013e3282f39703
PubMed Article Google Scholar
Kung S, Espinel Z, Lapid MI (2012) Treatment of nightmares with prazosin: a systematic review. Mayo Clin Proc 87(9):890–900. doi:10.1016/j.mayocp.2012.05.015
CAS PubMed PubMed Central Article Google Scholar
Lindberg N, Virkkunen M, Tani P, Appelberg B, Virkkala J, Rimon R, Porkka-Heiskanen T (2002) Effect of a single-dose of olanzapine on sleep in healthy females and males. Int Clin Psychopharmacol 17(4):177–184
CAS PubMed Article Google Scholar
Lipinska M, Timol R, Kaminer D, Thomas KG (2014) Disrupted rapid eye movement sleep predicts poor declarative memory performance in post-traumatic stress disorder. J Sleep Res 23(3):309–317. doi:10.1111/jsr.12122
PubMed Article Google Scholar
Maes J, Verbraecken J, Willemen M, De Volder I, van Gastel A, Michiels N, Verbeek I, Vandekerckhove M, Wuyts J, Haex B, Willemen T, Exadaktylos V, Bulckaert A, Cluydts R (2014) Sleep misperception, EEG characteristics and autonomic nervous system activity in primary insomnia: a retrospective study on polysomnographic data. Int J Psychophysiol 91(3):163–171. doi:10.1016/j.ijpsycho.2013.10.012
CAS PubMed Article Google Scholar
Maher MJ, Rego SA, Asnis GM (2006) Sleep disturbances in patients with post-traumatic stress disorder: epidemiology, impact and approaches to management. CNS Drugs 20(7):567–590. doi:10.2165/00023210-200620070-00003
CAS PubMed Article Google Scholar
Mandai O, Guerrien A, Sockeel P, Dujardin K, Leconte P (1989) REM sleep modifications following a Morse code learning session in humans. Physiol Behav 46(4):639–642. doi:10.1016/0031-9384(89)90344-2
CAS PubMed Article Google Scholar
Manoach DS, Stickgold R (2009) Does abnormal sleep impair memory consolidation in schizophrenia? Front Hum Neurosci 3:21. doi:10.3389/neuro.09.021.2009
PubMed PubMed Central Article Google Scholar
Manoach DS, Cain MS, Vangel MG, Khurana A, Goff DC, Stickgold R (2004) A failure of sleep-dependent procedural learning in chronic, medicated schizophrenia. Biol Psychiatry 56(12):951–956. doi:10.1016/j.biopsych.2004.09.012
PubMed Article Google Scholar
Manoach DS, Thakkar KN, Stroynowski E, Ely A, McKinley SK, Wamsley E, Djonlagic I, Vangel MG, Goff DC, Stickgold R (2010) Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages. J Psychiatr Res 44(2):112–120. doi:10.1016/j.jpsychires.2009.06.011
PubMed Article Google Scholar
Marshall L, Helgadottir H, Molle M, Born J (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444(7119):610–613. doi:10.1038/nature05278
CAS PubMed Article Google Scholar
Mayers AG, Baldwin DS (2005) Antidepressants and their effect on sleep. Hum Psychopharmacol 20(8):533–559. doi:10.1002/hup.726
CAS PubMed Article Google Scholar
Mednick S, Nakayama K, Stickgold R (2003) Sleep-dependent learning: a nap is as good as a night. Nat Neurosci 6(7):697–698. doi:10.1038/nn1078
CAS PubMed Article Google Scholar
Mednick SC, McDevitt EA, Walsh JK, Wamsley E, Paulus M, Kanady JC, Drummond SP (2013) The critical role of sleep spindles in hippocampal-dependent memory: a pharmacology study. J Neurosci 33(10):4494–4504. doi:10.1523/JNEUROSCI.3127-12.2013
CAS PubMed PubMed Central Article Google Scholar
Mellman TA, Kulick-Bell R, Ashlock LE, Nolan B (1995a) Sleep events among veterans with combat-related posttraumatic stress disorder. Am J Psychiatry 152(1):110–115
CAS PubMed Article Google Scholar
Mellman TA, Kumar A, Kulick-Bell R, Kumar M, Nolan B (1995b) Nocturnal/daytime urine noradrenergic measures and sleep in combat-related PTSD. Biol Psychiatry 38(3):174–179. doi:10.1016/0006-3223(94)00238-X
CAS PubMed Article Google Scholar
Mellman TA, Pigeon WR, Nowell PD, Nolan B (2007) Relationships between REM sleep findings and PTSD symptoms during the early aftermath of trauma. J Trauma Stress 20(5):893–901. doi:10.1002/jts.20246
PubMed Article Google Scholar
Menz MM, Rihm JS, Salari N, Born J, Kalisch R, Pape HC, Marshall L, Buchel C (2013) The role of sleep and sleep deprivation in consolidating fear memories. Neuroimage 75:87–96. doi:10.1016/j.neuroimage.2013.03.001
CAS PubMed Article Google Scholar
Monti JM, Monti D (2005) Sleep disturbance in schizophrenia. Int Rev Psychiatry 17(4):247–253. doi:10.1080/09540260500104516
PubMed Article Google Scholar
Monti JM, BaHammam AS, Pandi-Perumal SR, Bromundt V, Spence DW, Cardinali DP, Brown GM (2013) Sleep and circadian rhythm dysregulation in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 43:209–216. doi:10.1016/j.pnpbp.2012.12.021
PubMed Article Google Scholar
Morgan PT, Kehne JH, Sprenger KJ, Malison RT (2010) Retrograde effects of triazolam and zolpidem on sleep-dependent motor learning in humans. J Sleep Res 19(1 Pt 2):157–164. doi:10.1111/j.1365-2869.2009.00757.x
PubMed Article Google Scholar
Morgenthaler J, Wiesner CD, Hinze K, Abels LC, Prehn-Kristensen A, Göder R (2014) Selective REM-sleep deprivation does not diminish emotional memory consolidation in young healthy subjects. PLoS One 9(2):e89849. doi:10.1371/journal.pone.0089849
PubMed PubMed Central Article CAS Google Scholar
Ngo HV, Martinetz T, Born J, Molle M (2013) Auditory closed-loop stimulation of the sleep slow oscillation enhances memory. Neuron 78(3):545–553. doi:10.1016/j.neuron.2013.03.006
CAS PubMed Article Google Scholar
Nielsen T, Levin R (2007) Nightmares: a new neurocognitive model. Sleep Med Rev 11(4):295–310. doi:10.1016/j.smrv.2007.03.004
PubMed Article Google Scholar
Nissen C, Kloepfer C, Nofzinger EA, Feige B, Voderholzer U, Riemann D (2006) Impaired sleep-related memory consolidation in primary insomnia—a pilot study. Sleep 29(8):1068–1073
PubMed Google Scholar
Nissen C, Kloepfer C, Feige B, Piosczyk H, Spiegelhalder K, Voderholzer U, Riemann D (2011) Sleep-related memory consolidation in primary insomnia. J Sleep Res 20(1 Pt 2):129–136. doi:10.1111/j.1365-2869.2010.00872.x
PubMed Article Google Scholar
Pace-Schott EF, Hobson JA (2002) The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat Rev Neurosci 3(8):591–605. doi:10.1038/nrn895
CAS PubMed Article Google Scholar
Parrino L, Ferri R, Bruni O, Terzano MG (2012) Cyclic alternating pattern (CAP): the marker of sleep instability. Sleep Med Rev 16(1):27–45. doi:10.1016/j.smrv.2011.02.003
PubMed Article Google Scholar
Peppard PE, Szklo-Coxe M, Hla KM, Young T (2006) Longitudinal association of sleep-related breathing disorder and depression. Arch Intern Med 166(16):1709–1715. doi:10.1001/archinte.166.16.1709
PubMed Article Google Scholar
Perlis ML, Giles DE, Mendelson WB, Bootzin RR, Wyatt JK (1997) Psychophysiological insomnia: the behavioural model and a neurocognitive perspective. J Sleep Res 6(3):179–188
CAS PubMed Article Google Scholar
Perlis ML, Merica H, Smith MT, Giles DE (2001) Beta EEG activity and insomnia. Sleep Med Rev 5(5):363–374. doi:10.1053/smrv.2001.0151
PubMed Article Google Scholar
Phillips KG, Bartsch U, McCarthy AP, Edgar DM, Tricklebank MD, Wafford KA, Jones MW (2012) Decoupling of sleep-dependent cortical and hippocampal interactions in a neurodevelopmental model of schizophrenia. Neuron 76(3):526–533. doi:10.1016/j.neuron.2012.09.016
CAS PubMed PubMed Central Article Google Scholar
Pillai V, Kalmbach DA, Ciesla JA (2011) A meta-analysis of electroencephalographic sleep in depression: evidence for genetic biomarkers. Biol Psychiatry 70(10):912–919. doi:10.1016/j.biopsych.2011.07.016
PubMed Article Google Scholar
Pitman RK, Sanders KM, Zusman RM, Healy AR, Cheema F, Lasko NB, Cahill L, Orr SP (2002) Pilot study of secondary prevention of posttraumatic stress disorder with propranolol. Biol Psychiatry 51(2):189–192. doi:10.1016/S0006-3223(01)01279-3
CAS PubMed Article Google Scholar
Plante DT, Goldstein MR, Landsness EC, Peterson MJ, Riedner BA, Ferrarelli F, Wanger T, Guokas JJ, Tononi G, Benca RM (2013) Topographic and sex-related differences in sleep spindles in major depressive disorder: a high-density EEG investigation. J Affect Disord 146(1):120–125. doi:10.1016/j.jad.2012.06.016
CAS PubMed Article Google Scholar
Plihal W, Born J (1997) Effects of early and late nocturnal sleep on declarative and procedural memory. J Cognit Neurosci 9(4):534–547. doi:10.1162/jocn.1997.9.4.534
CAS Article Google Scholar
Poulin J, Daoust AM, Forest G, Stip E, Godbout R (2003) Sleep architecture and its clinical correlates in first episode and neuroleptic-naive patients with schizophrenia. Schizophr Res 62(1–2):147–153. doi:10.1016/S0920-9964(02)00346-8
PubMed Article Google Scholar
Poundja J, Sanche S, Tremblay J, Brunet A (2012) Trauma reactivation under the influence of propranolol: an examination of clinical predictors. Eur J Psychotraumatol. doi:10.3402/ejpt.v3i0.15470
PubMed PubMed Central Google Scholar
Preston AR, Eichenbaum H (2013) Interplay of hippocamus and prefrontal cortex in memory. Curr Biol 23(special issue):R764–R773. doi:10.106/j.cub.2013.05.041
CAS PubMed PubMed Central Article Google Scholar
Rasch B, Born J (2013) About sleep’s role in memory. Physiol Rev 93(2):681–766. doi:10.1152/physrev.00032.2012
CAS PubMed PubMed Central Article Google Scholar
Rasch B, Buchel C, Gais S, Born J (2007) Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315(5817):1426–1429. doi:10.1126/science.1138581
CAS PubMed Article Google Scholar
Rasch B, Pommer J, Diekelmann S, Born J (2009) Pharmacological REM sleep suppression paradoxically improves rather than impairs skill memory. Nat Neurosci 12(4):396–397. doi:10.1038/nn.2206
CAS PubMed Article Google Scholar
Rechtschaffen A, Kales A (1968) A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. US Government Printing Office, Washington
Google Scholar
Riemann D, Spiegelhalder K, Feige B, Voderholzer U, Berger M, Perlis M, Nissen C (2010) The hyperarousal model of insomnia: a review of the concept and its evidence. Sleep Med Rev 14(1):19–31. doi:10.1016/j.smrv.2009.04.002
PubMed Article Google Scholar
Rosa RR, Bonnet MH (2000) Reported chronic insomnia is independent of poor sleep as measured by electroencephalography. Psychosom Med 62(4):474–482
CAS PubMed Article Google Scholar
Röschke J, Mann K (2002) The sleep EEG’s microstructure in depression: alterations of the phase relations between EEG rhythms during REM and NREM sleep. Sleep Med 3(6):501–505. doi:10.106/S1389-9457(02)00134-X
PubMed Article Google Scholar
Ross RJ, Ball WA, Sullivan KA, Caroff SN (1989) Sleep disturbance as the hallmark of posttraumatic stress disorder. Am J Psychiatry 146(6):697–707
CAS PubMed Article Google Scholar
Rudoy JD, Voss JL, Westerberg CE, Paller KA (2009) Strengthening individual memories by reactivating them during sleep. Science 326(5956):1079. doi:10.1126/science.1179013
CAS PubMed PubMed Central Article Google Scholar
Salviati M, Pallagrosi M, Valeriani G, Carlone C, Todini L, Biondi M (2013) On the role of noradrenergic system in PTSD and related sleep disturbances. The use of terazosin in PTSD related nightmares: a case report. Clin Ter 164(2):133–137
CAS PubMed Google Scholar
Schabus M, Heib DP, Lechinger J, Griessenberger H, Klimesch W, Pawlizki A, Kunz AB, Sterman BM, Hoedlmoser K (2014) Enhancing sleep quality and memory in insomnia using instrumental sensorimotor rhythm conditioning. Biol Psychol 95:126–134. doi:10.1016/j.biopsycho.2013.02.020
PubMed Article Google Scholar
Seeck-Hirschner M, Baier PC, Sever S, Buschbacher A, Aldenhoff JB, Goder R (2010) Effects of daytime naps on procedural and declarative memory in patients with schizophrenia. J Psychiatr Res 44(1):42–47. doi:10.1016/j.jpsychires.2009.05.008
PubMed Article Google Scholar
Sharpley AL, Vassallo CM, Cowen PJ (2000) Olanzapine increases slow-wave sleep: evidence for blockade of central 5-HT(2C) receptors in vivo. Biol Psychiatry 47(5):468–470. doi:10.1016/S0006-3223(99)00273-5
CAS PubMed Article Google Scholar
Smith C (2001) Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med Rev 5(6):491–506
CAS PubMed Article Google Scholar
Smith CT, Nixon MR, Nader RS (2004) Posttraining increases in REM sleep intensity implicate REM sleep in memory processing and provide a biological marker of learning potential. Learn Mem 11(6):714–719. doi:10.1101/lm.74904
PubMed PubMed Central Article Google Scholar
Spoormaker VI, Montgomery P (2008) Disturbed sleep in post-traumatic stress disorder: secondary symptom or core feature? Sleep Med Rev 12(3):169–184. doi:10.1016/j.smrv.2007.08.008
PubMed Article Google Scholar
Squire LR, Zola SM (1996) Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci USA 93(24):13515–13522
CAS PubMed PubMed Central Article Google Scholar
Stein MB, Kerridge C, Dimsdale JE, Hoyt DB (2007) Pharmacotherapy to prevent PTSD: results from a randomized controlled proof-of-concept trial in physically injured patients. J Trauma Stress 20(6):923–932. doi:10.1002/jts.20270
PubMed Article Google Scholar
Stickgold R, Whidbee D, Schirmer B, Patel V, Hobson JA (2000) Visual discrimination task improvement: a multi-step process occurring during sleep. J Cognit Neurosci 12(2):246–254
CAS Article Google Scholar
Tempesta D, Mazza M, Iaria G, De Gennaro L, Ferrara M (2011) A specific deficit in spatial memory acquisition in post-traumatic stress disorder and the role of sleep in its consolidation. Hippocampus 22(5):1154–1163. doi:10.1002/hipo.20961
PubMed Article Google Scholar
Tononi G, Cirelli C (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 62(2):143–150. doi:10.1016/j.brainresbull.2003.09.004
PubMed Article Google Scholar
Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10(1):49–62. doi:10.1016/j.smrv.2005.05.002
PubMed Article Google Scholar
Vaiva G, Ducrocq F, Jezequel K, Averland B, Lestavel P, Brunet A, Marmar CR (2003) Immediate treatment with propranolol decreases posttraumatic stress disorder two months after trauma. Biol Psychiatry 54(9):947–949. doi:10.1016/S0006-3223(03)00412-8
CAS PubMed Article Google Scholar
Van Cauter E, Linkowski P, Kerkhofs M, Hubain P, L’Hermite-Baleriaux M, Leclercq R, Brasseur M, Copinschi G, Mendlewicz J (1991) Circadian and sleep-related endocrine rhythms in schizophrenia. Arch Gen Psychiatry 48(4):348–356
PubMed Article Google Scholar
van der Helm E, Walker MP (2012) Sleep and affective brain regulation. Soc Personal Psychol Compass 6:773–791
Article Google Scholar
van der Kolk B, Blitz R, Burr W, Sherry S, Hartmann E (1984) Nightmares and trauma: a comparison of nightmares after combat with lifelong nightmares in veterans. Am J Psychiatry 141(2):187–190
PubMed Article Google Scholar
van Kesteren MT, Ruiter DJ, Fernández G, Henson RN (2012) How schema and novelty augment memory formation. Trends Neurosci 35(4):211–219. doi:10.1016/j.tins.2012.02.001
PubMed Article CAS Google Scholar
van Liempt S (2012) Sleep disturbances and PTSD: a perpetual circle? Eur J Psychotraumatol. doi:10.3402/ejpt.v3i0.19142
PubMed PubMed Central Google Scholar
van Liempt S, Vermetten E, Lentjes E, Arends J, Westenberg H (2011) Decreased nocturnal growth hormone secretion and sleep fragmentation in combat-related posttraumatic stress disorder; potential predictors of impaired memory consolidation. Psychoneuroendocrinology 36(9):1361–1369. doi:10.1016/j.psyneuen.2011.03.009
PubMed Article CAS Google Scholar
van Liempt S, Arends J, Cluitmans PJ, Westenberg HG, Kahn RS, Vermetten E (2013a) Sympathetic activity and hypothalamo-pituitary-adrenal axis activity during sleep in post-traumatic stress disorder: a study assessing polysomnography with simultaneous blood sampling. Psychoneuroendocrinology 38(1):155–165. doi:10.1016/j.psyneuen.2012.05.015
PubMed Article CAS Google Scholar
van Liempt S, van Zuiden M, Westenberg H, Super A, Vermetten E (2013b) Impact of impaired sleep on the development of PTSD symptoms in combat veterans: a prospective longitudinal cohort study. Depress Anxiety 30(5):469–474. doi:10.1002/da.22054
PubMed Article Google Scholar
Vanderheyden WM, Poe GR, Liberzon I (2014) Trauma exposure and sleep: using a rodent model to understand sleep function in PTSD. Exp Brain Res 232(5):1575–1584. doi:10.1007/s00221-014-3890-4
PubMed Article Google Scholar
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. doi:10.1016/j.biopsych.2006.03.061
PubMed Article Google Scholar
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. doi:10.1016/S0896-6273(02)00746-8
CAS PubMed Article Google Scholar
Wamsley EJ, Tucker MA, Shinn AK, Ono KE, McKinley SK, Ely AV, Goff DC, Stickgold R, Manoach DS (2012) Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation? Biol Psychiatry 71(2):154–161. doi:10.1016/j.biopsych.2011.08.008
PubMed Article Google Scholar
Wamsley EJ, Shinn AK, Tucker MA, Ono KE, McKinley SK, Ely AV, Goff DC, Stickgold R, Manoach DS (2013) The effects of eszopiclone on sleep spindles and memory consolidation in schizophrenia: a randomized placebo-controlled trial. Sleep 36(9):1369–1376. doi:10.5665/sleep.2968
PubMed PubMed Central Google Scholar
Waters F, Manoach DS (2012) Sleep dysfunctions in schizophrenia: a practical review. Open J Psychiatry 2:384–392. doi:10.4236/ojpsych.2012.224054
Article Google Scholar
Wheaton AG, Perry GS, Chapman DP, Croft JB (2012) Sleep disordered breathing and depression among US adults: National Health and Nutrition Examination Survey, 2005–2008. Sleep 35(4):461–467. doi:10.5665/sleep.1724
PubMed PubMed Central Google Scholar
Woodward SH, Murburg MM, Bliwise DL (2000) PTSD-related hyperarousal assessed during sleep. Physiol Behav 70(1–2):197–203. doi:10.1016/S0031-9384(00)00271-7
CAS PubMed Article Google Scholar

Download references

Author information

Affiliations

German Center for Neurodegenerative Diseases (DZNE) Magdeburg, Leipziger Str. 44, 39120, Magdeburg, Germany
Monique Goerke & Notger G. Müller
Department of Psychiatry and Psychotherapy, University of Rostock, Gehlsheimer Str. 20, 18147, Rostock, Germany
Monique Goerke & Stefan Cohrs

Authors

Monique Goerke
View author publications
You can also search for this author in PubMed Google Scholar
Notger G. Müller
View author publications
You can also search for this author in PubMed Google Scholar
Stefan Cohrs
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Monique Goerke.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Goerke, M., Müller, N.G. & Cohrs, S. Sleep-dependent memory consolidation and its implications for psychiatry. J Neural Transm 124, 163–178 (2017). https://doi.org/10.1007/s00702-015-1476-3

Download citation

Received: 06 May 2015
Accepted: 20 October 2015
Published: 30 October 2015
Issue Date: February 2017
DOI: https://doi.org/10.1007/s00702-015-1476-3

Keywords

Sleep
Memory consolidation
Insomnia
Major depression
Schizophrenia
Post-traumatic stress disorder