Targeting sleep oscillations to improve memory in schizophrenia
Open accessAbstract
Although schizophrenia is defined by waking phenomena, a growing literature documents a deficit in sleep spindles, a defining oscillation of stage 2 non-rapid eye movement sleep. Compelling evidence supports an important role for spindles in cognition, and particularly memory. In schizophrenia, although the spindle deficit correlates with impaired sleep-dependent memory consolidation, recent clinical trials find that increasing spindles does not improve memory. This may reflect that sleep-dependent memory consolidation relies not on spindles alone, but also on their precise temporal coordination with cortical slow oscillations and hippocampal sharp-wave ripples. Consequently, interventions to improve memory in schizophrenia must not only increase spindles, but also preserve or enhance slow oscillations, hippocampal ripples and their temporal relations. Because hippocampal ripples and the activity of the thalamic spindle generator are difficult to measure noninvasively, screening potential interventions requires complementary animal and human studies. In this review we (i) propose that sleep oscillations are novel pathophysiological targets for therapy to improve cognition in schizophrenia; (ii) summarize our understanding of how these oscillations interact to consolidate memory; (iii) suggest that a systems neuroscience strategy is essential to selecting and evaluating effective treatments, and illustrate this with findings from clinical trials; and (iv) selectively review the interventional literature relevant to sleep and cognition, covering both pharmacological and noninvasive brain stimulation approaches. We conclude that coordinated sleep oscillations are promising targets for improving cognition in schizophrenia and that effective therapies will need to preserve or enhance sleep oscillatory dynamics and restore function at the network level.
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Closed-loop auditory stimulation has shown promise with clinical populations including people with schizophrenia, older adults, and children with ADHD.
“For example, closed-loop auditory stimulation has shown promise with clinical populations including people with schizophrenia [32] older adults [33], and children with ADHD [34].”
From Sleep and memory consolidation in healthy, neurotypical children, and adults: a summary of systematic reviews and meta-analyses. (2023) · cites this paper as [32]
In the section on noninvasive brain stimulation during sleep (page unavailable), the review reports promising results for closed-loop auditory stimulation, including in people with mild cognitive impairment. It does not report promising results in people with schizophrenia; instead, it says these methods have seldom been used in other clinical populations. The schizophrenia portion attributed to citation [32] is therefore unsupported. (LLM, conf=0.87)
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Cites
Biological insights from 108 schizophrenia-associated genetic loci
Schizophrenia Working Group of the Psychiatric Genomics Consortium (2014) · Nature · doi:10.1038/nature13595 · Cited by 7,577 · see citing works
(2007) · Cited by 6,530 · see citing works
Reactivation of hippocampal ensemble memories during sleep
Wilson, M. A., & McNaughton, B. L. (1994) · Science · doi:10.1126/science.8036517 · Cited by 3,118 · see citing works
Green, M. F., Kern, R. S., Braff, D. L., & Mintz, J. (2000) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033430 · Cited by 2,999 · see citing works
Boosting slow oscillations during sleep potentiates memory
Marshall, L., Helgadóttir, H., Mölle, M., & Born, J. (2006) · Nature · doi:10.1038/nature05278 · Cited by 1,792 · see citing works
Coordinated memory replay in the visual cortex and hippocampus during sleep
Ji, D., & Wilson, M. A. (2007) · Nature Neuroscience · doi:10.1038/nn1825 · Cited by 1,669 · see citing works
A technical guide to tDCS, and related non-invasive brain stimulation tools
Woods, A. J., Antal, A., Bikson, M., Boggio, P. S., Brunoni, A. R., Celnik, P. A., Cohen, L. G., Fregni, F., Herrmann, C. S., Kappenman, E. S., et al. (2015) · Clinical Neurophysiology · doi:10.1016/j.clinph.2015.11.012 · Cited by 1,450 · see citing works
Coordinated interactions between hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep
Siapas, A. G., & Wilson, M. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80629-7 · Cited by 1,052 · see citing works
Noninvasive Deep Brain Stimulation via Temporally Interfering Electric Fields
Grossman, N., Bono, D. C., Dedic, N., Kodandaramaiah, S. B., Rudenko, A., Suk, H., Cassara, A. M., Neufeld, E., Kuster, N., Tsai, L., et al. (2017) · Cell · doi:10.1016/j.cell.2017.05.024 · Cited by 996 · see citing works
Steriade, M., Nunez, A., & Amzica, F. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-08-03266.1993 · Cited by 894 · see citing works
Auditory closed-loop stimulation of the sleep slow oscillation enhances memory
Ngo, H.-V. V., Martinetz, T., Born, J., & Mölle, M. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.006 · Cited by 885 · see citing works
Staresina, B. P., Bergmann, T. O., Bonnefond, M., van der Meij, R., Jensen, O., Deuker, L., Elger, C. E., Axmacher, N., & Fell, J. (2015) · Nature Neuroscience · doi:10.1038/nn.4119 · Cited by 831 · see citing works
System consolidation of memory during sleep
Born, J., & Wilhelm, I. (2012) · Psychological Research · doi:10.1007/s00426-011-0335-6 · Cited by 667 · see citing works
Fogel, S. M., & Smith, C. T. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.003 · Cited by 628 · see citing works
Latchoumane, C.-F. V., Ngo, H.-V. V., Born, J., & Shin, H.-S. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.025 · Cited by 561 · see citing works
Transcranial direct current stimulation during sleep improves declarative memory
Marshall, L., Mölle, M., Hallschmid, M., & Born, J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.2725-04.2004 · Cited by 548 · see citing works
Gulsuner, S., Walsh, T., Watts, A. C., Lee, M. K., Thornton, A. M., Casadei, S., Rippey, C., Shahin, H., Braff, D., Cadenhead, K. S., et al. (2013) · Cell · doi:10.1016/j.cell.2013.06.049 · Cited by 536 · see citing works
Old brains come uncoupled in sleep: slow wave-spindle synchrony, brain atrophy, and forgetting
Helfrich, R. F., Mander, B. A., Jagust, W. J., Knight, R. T., & Walker, M. P. (2018) · Neuron · doi:10.1016/j.neuron.2017.11.020 · Cited by 497 · see citing works
Wamsley, E. J., Tucker, M. A., Shinn, A. K., Ono, K. E., McKinley, S. K., Ely, A. V., Goff, D. C., Stickgold, R., & Manoach, D. S. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.08.008 · Cited by 492 · see citing works
Self-citationWhy do we sleep?11Published on the World Wide Web on 7 November 2000.
Sejnowski, T. J., & Destexhe, A. (2000) · Brain Research · doi:10.1016/s0006-8993(00)03007-9 · Cited by 489 · see citing works
The Economic Burden of Schizophrenia in the United States in 2013
Cloutier, M., Aigbogun, M. S., Guérin, A., Nitulescu, R., Ramanakumar, A. V., Kamat, S., DeLucia, M., Duffy, R. A., Legacy, S. N., Henderson, C., et al. (2016) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.15m10278 · Cited by 479 · see citing works
Insel, T. R. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2008.540 · Cited by 459 · see citing works
Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans
Clemens, Z., Molle, M., Eross, L., Barsi, P., Halasz, P., & Born, J. (2007) · Brain · doi:10.1093/brain/awm146 · Cited by 398 · see citing works
Anticevic, A., Haut, K. M., Murray, J. D., Repovš, G., Yang, G., Diehl, C., McEwen, S. C., Bearden, C. E., Addington, J., Goodyear, B. G., et al. (2015) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2015.0566 · Cited by 381 · see citing works
Atypical sleep architecture and the autism phenotype
Limoges, É., Mottron, L., Bolduc, C., Berthiaume, C., & Godbout, R. (2005) · Brain · doi:10.1093/brain/awh425 · Cited by 351 · see citing works
Loomis, A. L., Harvey, E. N., & Hobart, G. (1938) · Journal of Neurophysiology · doi:10.1152/jn.1938.1.5.413 · Cited by 338 · see citing works
The Critical Role of Sleep Spindles in Hippocampal-Dependent Memory: A Pharmacology Study
Mednick, S. C., McDevitt, E. A., Walsh, J. K., Wamsley, E. J., Paulus, M. P., Kanady, J. C., & Drummond, S. P. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3127-12.2013 · Cited by 318 · see citing works
Spontaneous brain rhythms predict sleep stability in the face of noise
Dang‐Vu, T. T., McKinney, S. M., Buxton, O. M., Solet, J. M., & Ellenbogen, J. M. (2010) · Current Biology · doi:10.1016/j.cub.2010.06.032 · Cited by 297 · see citing works
Hippocampal interneurons are abnormal in schizophrenia
Konradi, C., Yang, C. K., Zimmerman, E. I., Lohmann, K. M., Gresch, P., Pantazopoulos, H., Berretta, S., & Heckers, S. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.06.007 · Cited by 288 · see citing works
Slow oscillations orchestrating fast oscillations and memory consolidation
Mölle, M., & Born, J. (2011) · Progress in Brain Research · doi:10.1016/b978-0-444-53839-0.00007-7 · Cited by 270 · see citing works
Lustenberger, C., Boyle, M. R., Alagapan, S., Mellin, J. M., Vaughn, B. V., & Frӧhlich, F. (2016) · Current Biology · doi:10.1016/j.cub.2016.06.044 · Cited by 260 · see citing works
Acoustic Enhancement of Sleep Slow Oscillations and Concomitant Memory Improvement in Older Adults
Papalambros, N. A., Santostasi, G., Malkani, R. G., Braun, R., Weintraub, S., Paller, K. A., & Zee, P. C. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00109 · Cited by 259 · cited 1× · see citing works
“Compared with sham stimulation, in multiple studies, closed-loop auditory stimulation during SO upstateswas associated with increased SO and fast-sigma power during SO upstates and improved sleep-dependent declarative memory consolidation (Leminen et al., 2017; Ngo et al., 2013; Ong et al., 2016; Ong et al., 2018; Pap…”
ResultNeuronal Nicotinic Receptors in Dementia with Lewy Bodies and Schizophrenia
COURT, J. A., Spurden, D., Lloyd, S. R., McKeith, I. G., Ballard, C. G., Cairns, N. J., Kerwin, R. W., Perry, R., & Perry, E. K. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0731590.x · Cited by 252 · see citing works
An electroencephalographic fingerprint of human sleep
De Gennaro, L., Ferrara, M., Vecchio, F., Curcio, G., & Bertini, M. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.01.020 · Cited by 247 · see citing works
Enhancement of sleep slow waves: underlying mechanisms and practical consequences
Bellesi, M., Riedner, B. A., Garcia-Molina, G. N., Cirelli, C., & Tononi, G. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00208 · Cited by 239 · see citing works
Ladenbauer, J., Ladenbauer, J., Külzow, N., de Boor, R., Avramova, E., Grittner, U., & Flöel, A. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0260-17.2017 · Cited by 220 · see citing works
Fine‐tuned coupling between human parahippocampal ripples and sleep spindles
Clemens, Z., Mölle, M., Erőss, L., Jakus, R., Rásonyi, G., Halász, P., & Born, J. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07505.x · Cited by 214 · see citing works
The Ca <sub>V</sub> 3.3 calcium channel is the major sleep spindle pacemaker in thalamus
Astori, S., Wimmer, R. D., Prosser, H. M., Corti, C., Corsi, M., Liaudet, N., Volterra, A., Franken, P., Adelman, J. P., & Lüthi, A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105115108 · Cited by 213 · see citing works
Manoach, D. S., Pan, J. Q., Purcell, S., & Stickgold, R. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.10.003 · Cited by 210 · see citing works
Self-citationHippocampal Pathology in Schizophrenia
Heckers, S., & Konradi, C. L. (2010) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_43 · Cited by 208 · see citing works
New views of the thalamic reticular nucleus in the adult and the developing brain
Mitrofanis, J., & Guillery, R. W. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90163-g · Cited by 205 · see citing works
Thalamic reticular impairment underlies attention deficit in Ptchd1Y/− mice
Wells, M. F., Wimmer, R. D., Schmitt, L. I., Feng, G., & Halassa, M. M. (2016) · Nature · doi:10.1038/nature17427 · Cited by 204 · see citing works
Lafon, B., Henin, S. E., Huang, Y., Friedman, D. J., Melloni, L., Thesen, T., Doyle, W., Buzsáki, G., Devinsky, O., Parra, L. C., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01045-x · Cited by 200 · see citing works
Smith, R. E., Haroutunian, V. H., Davis, K. L., & Meador‐Woodruff, J. H. (2001) · American Journal of Psychiatry · doi:10.1176/appi.ajp.158.9.1393 · Cited by 190 · see citing works
Marshall, L., Kirov, R., Brade, J., Mölle, M., & Born, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016905 · Cited by 188 · see citing works
Individual 'Fingerprints' in Human Sleep EEG Topography
Finelli, L. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00320-7 · Cited by 184 · see citing works
Sleep spindles in Parkinson's disease may predict the development of dementia
Latreille, V., Carrier, J., Lafortune, M., Postuma, R. B., Bertrand, J., Panisset, M., Chouinard, S., & Gagnon, J. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.09.009 · Cited by 179 · see citing works
Clemens, Z., Fabó, D., & Halász, P. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.04.035 · Cited by 179 · see citing works
Steullet, P., Cabungcal, J.-H., Bukhari, S. A., Ardelt, M., Pantazopoulos, H., Hamati, F., Salt, T. E., Cuénod, M., Kim, Q., & Berretta, S. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.230 · Cited by 170 · see citing works
Buchanan, R. W., Freedman, R., Javitt, D. C., Abi‐Dargham, A., & Lieberman, J. A. (2007) · Schizophrenia Bulletin · doi:10.1093/schbul/sbm083 · Cited by 169 · see citing works
Ong, J. L., Lo, J. C.-Y., Chee, N. I. Y. N., Santostasi, G., Paller, K. A., Zee, P. C., & Chee, M. W. L. (2015) · Sleep Medicine · doi:10.1016/j.sleep.2015.10.016 · Cited by 167 · see citing works
Gorgoni, M., Lauri, G., Truglia, I., Cordone, S., Sarasso, S., Scarpelli, S., Mangiaruga, A., D’Atri, A., Tempesta, D., Ferrara, M., et al. (2016) · Neural Plasticity · doi:10.1155/2016/8376108 · Cited by 162 · see citing works
Enhanced Memory Consolidation Via Automatic Sound Stimulation During Non-REM Sleep
Leminen, M., Virkkala, J., Saure, E., Paajanen, T. I., Zee, P. C., Santostasi, G., Hublin, C., Müller, K., Porkka‐Heiskanen, T., Huotilainen, M., et al. (2017) · SLEEP · doi:10.1093/sleep/zsx003 · Cited by 161 · see citing works
Memory improvement via slow-oscillatory stimulation during sleep in older adults
Westerberg, C. E., Florczak, S. M., Weıntraub, S., Mesulam, M. M., Marshall, L., Zee, P. C., & Paller, K. A. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.05.014 · Cited by 159 · see citing works
Ketz, N., Jones, A. P., Bryant, N. B., Clark, V. P., & Pilly, P. K. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0273-18.2018 · Cited by 157 · see citing works
Abnormal sleep spindles, memory consolidation, and schizophrenia
Manoach, D. S., & Stickgold, R. (2019) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-050718-095754 · Cited by 157 · see citing works
Self-citationKaestner, E. J., Wixted, J. T., & Mednick, S. C. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00433 · Cited by 149 · see citing works
Low-Intensity Transcranial Current Stimulation in Psychiatry
Philip, N. S., Nelson, B. G., Frӧhlich, F., Lim, K. O., Widge, A. S., & Carpenter, L. L. (2017) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2017.16090996 · Cited by 139 · see citing works
Coupling of Thalamocortical Sleep Oscillations Are Important for Memory Consolidation in Humans
Niknazar, M., Krishnan, G., Bazhenov, M., & Mednick, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0144720 · Cited by 138 · see citing works
Eggert, T., Dorn, H., Sauter, C., Nitsche, M. A., Bajbouj, M., & Danker-Hopfe, H. (2013) · Brain stimulation · doi:10.1016/j.brs.2013.05.006 · Cited by 125 · see citing works
Phillips, K. G., Bartsch, U., McCarthy, A. P., Edgar, D. M., Tricklebank, M. D., Wafford, K. A., & Jones, M. W. (2012) · Neuron · doi:10.1016/j.neuron.2012.09.016 · Cited by 124 · see citing works
Bódizs, R., Körmendi, J., Rigó, P., & Lázár, A. S. (2008) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2008.11.006 · Cited by 119 · see citing works
Cortical development, electroencephalogram rhythms, and the sleep/wake cycle
Cirelli, C., & Tononi, G. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.12.017 · Cited by 117 · see citing works
Thalamic Reticular Dysfunction as a Circuit Endophenotype in Neurodevelopmental Disorders
Krol, A., Wimmer, R. D., Halassa, M. M., & Feng, G. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.021 · Cited by 117 · see citing works
Acoustic enhancement of sleep slow oscillations in mild cognitive impairment
Papalambros, N. A., Weıntraub, S., Chen, T. Y., Grimaldi, D., Santostasi, G., Paller, K. A., Zee, P. C., & Malkani, R. G. (2019) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.796 · Cited by 114 · see citing works
Impaired Hippocampal Ripple-Associated Replay in a Mouse Model of Schizophrenia
Suh, J., Foster, D. J., Davoudi, H., Wilson, M. A., & Tonegawa, S. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.014 · Cited by 113 · see citing works
Wamsley, E. J., Shinn, A. K., Tucker, M. A., Ono, K. E., McKinley, S. K., Ely, A. V., GOFF, D. C., Stickgold, R., & Manoach, D. S. (2013) · SLEEP · doi:10.5665/sleep.2968 · Cited by 111 · see citing works
Self-citationDysfunctional Thalamus-Related Networks in Schizophrenia
Pinault, D. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq165 · Cited by 105 · see citing works
Göder, R., Baier, P. C., Beith, B., Baecker, C., Seeck-Hirschner, M., Junghanns, K., & Marshall, L. (2013) · Schizophrenia Research · doi:10.1016/j.schres.2012.12.014 · Cited by 101 · see citing works
Ladenbauer, J., Külzow, N., Paßmann, S., Antonenko, D., Grittner, U., Tamm, S., & Flöel, A. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.06.057 · Cited by 94 · see citing works
Schapiro, A. C., Reid, A. G., Morgan, A., Manoach, D. S., Verfaellie, M., & Stickgold, R. (2019) · Hippocampus · doi:10.1002/hipo.23101 · Cited by 94 · see citing works
Self-citationDemanuele, C., Bartsch, U., Baran, B., Khan, S., Vangel, M. G., Cox, R., Hämäläinen, M., Jones, M. W., Stickgold, R., & Manoach, D. S. (2016) · SLEEP · doi:10.1093/sleep/zsw013 · Cited by 91 · see citing works
Self-citationIntelligence measures and stage 2 sleep in typically-developing and autistic children
Tessier, S., Lambert, A., Chicoine, M., Scherzer, P. B., Soulières, I., & Godbout, R. (2015) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2015.05.003 · Cited by 84 · see citing works
Ong, J. L., Patanaik, A., Chee, N. I. Y. N., Lee, X. K., Poh, J.-H., & Chee, M. W. L. (2018) · SLEEP · doi:10.1093/sleep/zsy031 · Cited by 83 · see citing works
Tamaki, M., Huang, T.-R., Yotsumoto, Y., Hämäläinen, M., Lin, F., Náñez, J. E., Watanabe, T., & Sasaki, Y. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1198-13.2013 · Cited by 81 · see citing works
Paßmann, S., Külzow, N., Ladenbauer, J., Antonenko, D., Grittner, U., Tamm, S., & Flöel, A. (2016) · Brain stimulation · doi:10.1016/j.brs.2016.04.016 · Cited by 79 · see citing works
Baran, B., Karahanoğlu, F. I., Mylonas, D., Demanuele, C., Vangel, M. G., Stickgold, R., Anticevic, A., & Manoach, D. S. (2019) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2019.04.012 · Cited by 76 · see citing works
Self-citationSahlem, G. L., Badran, B. W., Halford, J. J., Williams, N., Korte, J. E., Leslie, K., Strachan, M. K., Breedlove, J. L., Runion, J., Bachman, D., et al. (2015) · Brain stimulation · doi:10.1016/j.brs.2015.01.414 · Cited by 75 · see citing works
Weigenand, A., Mölle, M., Werner, F., Martinetz, T., & Marshall, L. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13334 · Cited by 74 · see citing works
A rare schizophrenia risk variant of CACNA1I disrupts CaV3.3 channel activity
Andrade, A., Hope, J. M., Allen, A., Yorgan, V. A., Lipscombe, D., & Pan, J. Q. (2016) · Scientific Reports · doi:10.1038/srep34233 · Cited by 74 · see citing works
Barham, M. P., Enticott, P. G., Conduit, R., & Lum, J. A. G. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.01.009 · Cited by 74 · see citing works
Sleep spindles are locally modulated by training on a brain–computer interface
Johnson, L. A., Blakely, T. M., Hermes, D., Hakimian, S., Ramsey, N. F., & Ojemann, J. G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1207532109 · Cited by 73 · see citing works
Spindle activity in young children with autism, developmental delay, or typical development
Farmer, C., Chilakamarri, P., Thurm, A. E., Swedo, S. E., Holmes, G. L., & Buckley, A. W. (2018) · Neurology · doi:10.1212/wnl.0000000000005759 · Cited by 73 · see citing works
Garside, P., Arizpe, J. M., Lau, C. I., Goh, C. C. W., & Walsh, V. (2015) · Brain stimulation · doi:10.1016/j.brs.2014.12.010 · Cited by 69 · see citing works
Large-scale structure and individual fingerprints of locally coupled sleep oscillations
Cox, R., Mylonas, D., Manoach, D. S., & Stickgold, R. (2018) · SLEEP · doi:10.1093/sleep/zsy175 · Cited by 67 · see citing works
Self-citationMylonas, D., Baran, B., Demanuele, C., Cox, R., Vuper, T. C., Seicol, B. J., Fowler, R., Correll, D., Parr, E., Callahan, C. E., et al. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-00833-2 · Cited by 64 · see citing works
Self-citationLocation specific sleep spindle activity in the early visual areas and perceptual learning
Bang, J. W., Khalilzadeh, O., Hämäläinen, M., Watanabe, T., & Sasaki, Y. (2014) · Vision Research · doi:10.1016/j.visres.2013.12.014 · Cited by 60 · see citing works
Tek, C., Palmese, L. B., Krystal, A. D., Srihari, V. H., DeGeorge, P. C., Reutenauer, E. L., & Guloksuz, S. (2014) · Schizophrenia Research · doi:10.1016/j.schres.2014.10.002 · Cited by 59 · cited 1× · see citing works
“In a placebo-controlled trial that did not include polysomnography, eszopiclone (Lunesta), a non-benzodiazepine sedative hypnotic, improved working memory in schizophrenia, but not symptoms (Tek et al., 2014).”
BackgroundSpindle activity orchestrates plasticity during development and sleep
Lindemann, C., Ahlbeck, J., Bitzenhofer, S. H., & Hanganu-Opatz, I. L. (2016) · Neural Plasticity · doi:10.1155/2016/5787423 · Cited by 59 · see citing works
Insights on auditory closed-loop stimulation targeting sleep spindles in slow oscillation up-states
Ngo, H.-V. V., Seibold, M., Boche, D. C., Mölle, M., & Jan Born, A. (2018) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2018.09.006 · Cited by 57 · see citing works
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Schizophrenia, IX: Cognition in Schizophrenia—The MATRICS Initiative
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Bueno‐Lopez, A., Eggert, T., Dorn, H., & Danker‐Hopfe, H. (2019) · Brain stimulation · doi:10.1016/j.brs.2019.02.012 · Cited by 44 · see citing works
Donoso, J. R., Schmitz, D., Maier, N., & Kempter, R. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0188-17.2018 · Cited by 43 · see citing works
Evrard, A., & Ropert, N. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1671-09.2009 · Cited by 37 · see citing works
Kokkinos, V., & Kostopoulos, G. (2010) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2010.00830.x · Cited by 34 · see citing works
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Interhemispheric Interactions of the Human Thalamic Reticular Nucleus
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Flagged first, then by citations
Research works printed but not linked: 2
- Scolnick E, Pan J, 2017 CACNA1I: A Potential Novel Target for Schizophrenia Motivated by Emerging Human genetics. Schizophrenia Bulletin 43(Issue suppl_1), S63.
- Sejnowski TJ, Destexhe A, 2000 Why do we sleep? Brain Res 886(1–2), 208– 223. 11119697
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Schizophrenia, other neuropsychiatric disorders and sleep
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Self-citation
- Authors
- Manoach, D. S., Mylonas, D., & Baxter, B.
- Affiliations
- Harvard University (US)
- Corresponding author
- Manoach, Dara S.
- Venue
- Schizophrenia Research
- Publisher
- Elsevier BV
- Published
- 2020-07
- Volume
- 221
- Pages
- 63-70
- ISSN
- 0920-9964 (ISSN-L)
- PMC
- PMC7316628
- OpenAlex
- W3003390330
- Cited by
- 36
- References
- 102
- Citations by year
- 2025: 5 · 2024: 4 · 2023: 8 · 2022: 8 · 2021: 6 · 2020: 5
- FWCI
- 3.63
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Schizophrenia Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health
- National Heart Lung and Blood Institute
- National Center for Research Resources
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- schizophrenia, sleep spindles
- MeSH terms
- Memory Consolidation, Animals, Electroencephalography, Hippocampus, Humans, Memory, Schizophrenia, Sleep, Sleep Stages
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