Top

Published in:

01-02-2017 | Psychiatry and Preclinical Psychiatric Studies - Review Article

Sleep-dependent memory consolidation and its implications for psychiatry

Authors: Monique Goerke, Notger G. Müller, Stefan Cohrs

Published in: Journal of Neural Transmission | Special Issue 1/2017

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.

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).

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 PubMedCrossRef

American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. American Psychiatric Publishing, ArlingtonCrossRef

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

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 PubMedPubMedCentralCrossRef

Armitage R, Hoffmann RF, Rush AJ (1999) Biological rhythm disturbance in depression: temporal coherence of ultradian sleep EEG rhythms. Psychol Med 29(6):1435–1448PubMedCrossRef

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 PubMedCrossRef

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 CrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentral

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

Caldwell DF, Domino EF (1967) Electroencephalographic and eye movement patterns during sleep in chronic schizophrenic patients. Electroencephalogr Clin Neurophysiol 22(5):414–420PubMedCrossRef

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 PubMedCrossRef

Chouinard S, Poulin J, Stip E, Godbout R (2004) Sleep in untreated patients with schizophrenia: a meta-analysis. Schizophr Bull 30(4):957–967PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

De Gennaro L, Ferrara M (2003) Sleep spindles: an overview. Sleep Med Rev 7(5):423–440. doi:10.1053/smrv.2002.0252 PubMedCrossRef

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 PubMedCrossRef

de Maertelaer V, Hoffman G, Lemaire M, Mendlewicz J (1987) Sleep spindle activity changes in patients with affective disorders. Sleep 10(5):443–451PubMed

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 CrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11(2):114–126. doi:10.1038/nrn2762 PubMed

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentral

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedPubMedCentralCrossRef

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

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 PubMedPubMedCentral

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

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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

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

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 PubMedPubMedCentral

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 PubMedPubMedCentralCrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedPubMedCentralCrossRef

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):797–802PubMedCrossRef

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):1401–1408PubMedPubMedCentral

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentral

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

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):1365–1375PubMed

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 CrossRef

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):679–682PubMedCrossRef

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):443–448PubMedCrossRef

Kessler RC, Sonnega A, Bromet E, Hughes M, Nelson CB (1995) Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry 52(12):1048–1060PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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):177–184PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

Mayers AG, Baldwin DS (2005) Antidepressants and their effect on sleep. Hum Psychopharmacol 20(8):533–559. doi:10.1002/hup.726 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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):110–115PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

Monti JM, Monti D (2005) Sleep disturbance in schizophrenia. Int Rev Psychiatry 17(4):247–253. doi:10.1080/09540260500104516 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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):1068–1073PubMed

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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):179–188PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 CrossRef

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 PubMedCrossRef

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 PubMedPubMedCentral

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 PubMedPubMedCentralCrossRef

Rasch B, Born J (2013) About sleep’s role in memory. Physiol Rev 93(2):681–766. doi:10.1152/physrev.00032.2012 PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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

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 PubMedCrossRef

Rosa RR, Bonnet MH (2000) Reported chronic insomnia is independent of poor sleep as measured by electroencephalography. Psychosom Med 62(4):474–482PubMedCrossRef

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 PubMedCrossRef

Ross RJ, Ball WA, Sullivan KA, Caroff SN (1989) Sleep disturbance as the hallmark of posttraumatic stress disorder. Am J Psychiatry 146(6):697–707PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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):133–137PubMed

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

Smith C (2001) Sleep states and memory processes in humans: procedural versus declarative memory systems. Sleep Med Rev 5(6):491–506PubMedCrossRef

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 PubMedPubMedCentralCrossRef

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 PubMedCrossRef

Squire LR, Zola SM (1996) Structure and function of declarative and nondeclarative memory systems. Proc Natl Acad Sci USA 93(24):13515–13522PubMedPubMedCentralCrossRef

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 PubMedCrossRef

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):246–254CrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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):348–356PubMedCrossRef

van der Helm E, Walker MP (2012) Sleep and affective brain regulation. Soc Personal Psychol Compass 6:773–791CrossRef

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):187–190PubMedCrossRef

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 PubMedCrossRef

van Liempt S (2012) Sleep disturbances and PTSD: a perpetual circle? Eur J Psychotraumatol. doi:10.3402/ejpt.v3i0.19142 PubMedPubMedCentral

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedCrossRef

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 PubMedPubMedCentral

Waters F, Manoach DS (2012) Sleep dysfunctions in schizophrenia: a practical review. Open J Psychiatry 2:384–392. doi:10.4236/ojpsych.2012.224054 CrossRef

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 PubMedPubMedCentral

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 PubMedCrossRef

Title: Sleep-dependent memory consolidation and its implications for psychiatry
Authors: Monique Goerke
Notger G. Müller
Stefan Cohrs
Publication date: 01-02-2017
Publisher: Springer Vienna
Published in: Journal of Neural Transmission / Issue Special Issue 1/2017
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-015-1476-3

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Sleep-dependent memory consolidation and its implications for psychiatry

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Special Issue 1/2017

Sleep and inflammatory markers in different psychiatric disorders

Electronic media use and insomnia complaints in German adolescents: gender differences in use patterns and sleep problems

Sleep recordings in individuals with borderline personality disorder before and after trauma therapy

Sustained attention in adult ADHD: time-on-task effects of various measures of attention

How does healthy aging impact on the circadian clock?

Blink rate and blink timing in children with ADHD and the influence of stimulant medication