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Reduced Sleep Spindle Activity in Schizophrenia Patients
Abstract
Objective: High-density EEG during sleep represents a powerful new tool to reveal potential abnormalities in rhythm-generating mechanisms while avoiding confounding factors associated with waking activities. As a first step in this direction, the authors employed high-density EEG to explore whether sleep rhythms differ between schizophrenia subjects, healthy individuals, and a psychiatric control group with a history of depression. Method: Healthy comparison subjects (N=17), medicated schizophrenia patients (N=18), and subjects with a history of depression (N=15) were recruited. Subjects were recorded during the first sleep episode of the night with a 256-electrode high-density EEG. Recordings were analyzed for changes in EEG power spectra, power topography, and sleep-specific cortical oscillations. Results: The authors found that the schizophrenia group had a significant reduction in centroparietal EEG power, from 13.75 to 15.00 Hz, in relation to both the comparison and depression groups. No significant difference in EEG power between the comparison and depression groups was identified. The authors also found a decrease in sleep spindle number, amplitude, duration, and integrated spindle activity in schizophrenia patients. Furthermore, integrated spindle activity had an effect size corresponding to 93.0% or 90.2% separation of the schizophrenia from the comparison or depression group. Conclusions: Sleep spindles are generated by the thalamic reticular nucleus in conjunction with specific thalamic nuclei and are modulated by corticothalamic and thalamocortical connections. The deficit in sleep spindles in schizophrenia subjects may reflect dysfunction in thalamic-reticular and thalamocortical mechanisms and could represent a biological marker of illness.
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“For example, over 90% of schizophrenic subjects show a dramatic reduction in sleep spindles, suggesting dysfunction in the reticular nucleus of the thalamus (Ferrarelli et al., 2007).”
From Biological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges (2009) · cites this paper as Ferrarelli et al., 2007
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Sleep Spindles in Humans: Insights from Intracranial EEG and Unit Recordings
Andrillon, T., Nir, Y., Staba, R. J., Ferrarelli, F., Cirelli, C., Tononi, G., & Fried, I. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.2604-11.2011 · Cited by 504
“While it should be noted that our sampling was mostly limited to medial brain areas, scalp topography suggests that human spindle activity is maximal at midline regions (Ferrarelli et al., 2007), thereby making our data particularly well suited to examine sleep spindles.”
BackgroundMethodSelf-citationSleep spindle activity is associated with the integration of new memories and existing knowledge
Tamminen, J., Payne, J. D., Stickgold, R., Wamsley, E. J., & Gaskell, M. G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3028-10.2010 · Cited by 478
“Automated detection (Ferrarelli et al., 2007) derived the number of discrete spindle events: for each channel, amplitude fluctuations in the filtered time series exceeding a predetermined threshold counted as spindles.”
BackgroundAcoustic 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
“Spindle detection was done as described by Ferrarelli et al. (2007) using the Hilbert transform to calculate spindle amplitude envelopes in channel Fpz.”
BackgroundMethodGenzel, L., Kroes, M. C. W., Dresler, M., & Battaglia, F. P. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.10.002 · Cited by 285
Benca, R. M., & Peterson, M. J. (2008) · Sleep Medicine · doi:10.1016/s1389-9457(08)70010-8 · Cited by 259
“The first application of hd-EEG sleep recording in psychiatry was in patients with schizophrenia, who showed reduced spindle activity in centroparietal regions compared to normal controls and patients with depression [55].”
BackgroundSelf-citationThe Thalamic Reticular Nucleus and Schizophrenia
Ferrarelli, F., & Tononi, G. (2010) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq142 · Cited by 244
“71,72 An initial study found that 18 schizophrenics had marked deficits in TRN-generated NREM sleep spindles.”
BackgroundSelf-citationIndividual Differences in Frequency and Topography of Slow and Fast Sleep Spindles
Cox, R., Schapiro, A. C., Manoach, D. S., & Stickgold, R. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00433 · Cited by 195
Form and function of sleep spindles across the lifespan
Clawson, B. C., Durkin, J., & Aton, S. J. (2016) · Neural Plasticity · doi:10.1155/2016/6936381 · Cited by 178
“Spindles are reduced in density, amplitude, and duration in schizophrenia patients who are either medicated [138–140] or drug-näıve [141].”
BackgroundHeritability of Sleep Electroencephalogram
Ambrosius, U., Lietzenmaier, S., Wehrle, R., Wichniak, A., Kalus, S., Winkelmann, J., Bettecken, T., Holsboer, F., Yassouridis, A., & Frieß, E. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.03.002 · Cited by 163
Involvement of spindles in memory consolidation is slow wave sleep-specific
Cox, R., Hofman, W. F., & Talamini, L. M. (2012) · Learning & Memory · doi:10.1101/lm.026252.112 · Cited by 163
“Sleep spindles were identified by a dynamic detection algorithm implemented in MATLAB (2007b, the Mathworks, Natick), closely resembling one described earlier (Ferrarelli et al. 2007).”
MethodReduced Natural Oscillatory Frequency of Frontal Thalamocortical Circuits in Schizophrenia
Ferrarelli, F., Sarasso, S., Bodien, Y. G., Riedner, B. A., Peterson, M. J., Bellesi, M., Massimini, M., Postle, B. R., & Tononi, G. (2012) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2012.147 · Cited by 163
“The TRN is also the pacemaker of sleep spindles, a non– rapid eye movement sleep fast oscillation, and 2 recent studies found marked deficits in the spindle activity of patients with schizophrenia compared with healthy and psychiatric control subjects.(61,62) Thus, the TRN, which is strategically placed between the co…”
ResultSelf-citationThe role of sleep spindles and slow-wave activity in integrating new information in semantic memory
Tamminen, J., Lambon Ralph, M. A., & Lewis, P. A. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.5093-12.2013 · Cited by 152
“Automated detection (Ferrarelli et al., 2007) derived the number of discrete spindle events: for each channel, amplitude fluctuations in the filtered time series exceeding a predetermined threshold counted as spindles.”
BackgroundGorgoni, 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
Individual Differences in White Matter Diffusion Affect Sleep Oscillations
Piantoni, G., Poil, S., Linkenkaer‐Hansen, K., Verweij, I. M., Ramautar, J. R., Someren, E. J. W. V., & van der Werf, Y. D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2030-12.2013 · Cited by 163
Dreaming in NREM Sleep: A High-Density EEG Study of Slow Waves and Spindles
Siclari, F., Bernardi, G., Cataldi, J., & Tononi, G. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.0855-18.2018 · Cited by 143
“Spindle detection was based on an automatic algorithm, adapted from a previous study (Ferrarelli et al., 2007).”
MethodSelf-citationManoach, D. S., Thakkar, K. N., Stroynowski, E., Ely, A. V., McKinley, S. K., Wamsley, E. J., Djonlagic, I. E., Vangel, M. G., GOFF, D. C., & Stickgold, R. (2009) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2009.06.011 · Cited by 154
“Studies of schizophrenia show reduced spindle activity (Ferrarelli et al., 2007), and positive relations between Stage 2 spindle density and verbal declarative memory performance (Goder et al., 2008).”
BackgroundManoach, D. S., Demanuele, C., Wamsley, E. J., Vangel, M. G., Montrose, D. M., Miewald, J. M., Kupfer, D. J., Buysse, D. J., Stickgold, R., & Keshavan, M. S. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00762 · Cited by 160
Sensory Pathways and Emotional Context for Action in Primate Prefrontal Cortex
Barbas, H., Zikopoulos, B., & Timbie, C. M. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.08.008 · Cited by 152
Sleep-Dependent Facilitation of Episodic Memory Details
van der Helm, E., Gujar, N., Nishida, M., & Walker, M. P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027421 · Cited by 138
“edu/eeglab/]) into either fast (13–15 Hz) spindle or slow (11– 13 Hz) spindle [53,54] bands, similar to previously reported fast and slow spindle analyses [21,22].”
BackgroundMethodSleep Spindle Density Predicts the Effect of Prior Knowledge on Memory Consolidation
Hennies, N., Ralph, M. A. L., Kempkes, M., Cousins, J. N., & Lewis, P. A. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3162-15.2016 · Cited by 149
“Automated detection (Ferrarelli et al., 2007), which has been widely used in the literature (Tamminen et al., 2013), derived the number of discrete spindle events.”
MethodBiological rhythms, higher brain function, and behavior: Gaps, opportunities, and challenges
Benca, R., Duncan, M. J., Frank, E., McClung, C., Nelson, R. J., & Vicentic, A. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.09.005 · Cited by 125
“For example, over 90% of schizophrenic subjects show a dramatic reduction in sleep spindles, suggesting dysfunction in the reticular nucleus of the thalamus (Ferrarelli et al., 2007).”
BackgroundDysfunctional Thalamus-Related Networks in Schizophrenia
Pinault, D. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq165 · Cited by 105
Cued memory reactivation during slow-wave sleep promotes explicit knowledge of a motor sequence
Cousins, J. N., El-Deredy, W., Parkes, L. M., Hennies, N., & Lewis, P. A. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1011-14.2014 · Cited by 92
“An automated detection algorithm (Ferrarelli et al., 2007) determined the number of spindle events at each electrode.”
MethodSlow Oscillations during Sleep Coordinate Interregional Communication in Cortical Networks
Cox, R., van Driel, J., de Boer, M., & Talamini, L. M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1953-14.2014 · Cited by 103
“Definitive evidence regarding the differential SO modulation of fast and slow spindles at the network level could be obtained using algorithms for the detection of individual spindles (Ferrarelli et al., 2007; Cox et al., 2014a).”
MethodStructural brain correlates of human sleep oscillations
Saletin, J. M., van der Helm, E., & Walker, M. P. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.06.021 · Cited by 93
“While no memory tasks were included in the present study, this identified relationship is consistent with a broad collection of pathological circumstances describing not only marked impairments in sleep spindle activity, but co-occurring deficits in hippocampal gray matter and episodic memory, including Alzheimer's di…”
Wimmer, R. D., Astori, S., Bond, C. T., Rovó, Z., Chatton, J.-Y., Adelman, J. P., Franken, P., & Lüthi, A. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2313-12.2012 · Cited by 90
“The study motivates further exploration of nRt function as a locus for improving sleep, including in the context of some neuropsychiatric conditions associated with decreased spindle activity (Ferrarelli et al., 2007).”
Does abnormal sleep impair memory consolidation in schizophrenia?
Manoach, D. S. (2009) · Frontiers in Human Neuroscience · doi:10.3389/neuro.09.021.2009 · Cited by 93
“There have also been mixed reports of changes in sleep spindles, including increased spindle counts (Hiatt et al., 1985), and both unchanged (Poulin et al., 2003) and reduced (Ferrarelli et al., 2007) sleep spindle density.”
Comparison of Sleep Spindles and Theta Oscillations in the Hippocampus
Sullivan, D. W., Mizuseki, K., Sorgi, A., & Buzsáki, G. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0552-13.2014 · Cited by 99
“Altered sleep spindle dynamics have been documented in several forms of mental disease (Ferrarelli et al., 2007, 2010; Vukadinovic, 2011; Wamsley et al., 2012; Wilson and Argyropoulos, 2012; Plante et al., 2013).”
Reduced Sleep Spindle Activity in Early-Onset and Elevated Risk for Depression
López, J., Hoffmann, R. F., & Armitage, R. (2010) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2010.05.014 · Cited by 90
Ripples Make Waves: Binding Structured Activity and Plasticity in Hippocampal Networks
Sadowski, J. H. L. P., Jones, M. W., & Mellor, J. R. (2011) · Neural Plasticity · doi:10.1155/2011/960389 · Cited by 84
“Changes in the structure of sleep and particularly reduced slow wave sleep and spindle activity are reliably observed in schizophrenic patients [121, 122], such deficits may contribute to the cognitive impairment seen in some individuals.”
BackgroundEffects of daytime naps on procedural and declarative memory in patients with schizophrenia
Seeck-Hirschner, M., Baier, P. C., Sever, S., Buschbacher, A., Aldenhoff, J. B., & Göder, R. (2009) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2009.05.008 · Cited by 75
Circadian Rhythms of Perineuronal Net Composition
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Riga, M. S., Sòria, G., Tudela, R., Artigas, F., & Celada, P. (2014) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145714000261 · Cited by 76
Ray, L. B., Sockeel, S., Soon, M., Boré, A., Myhr, A., Stojanoski, B. B., Cusack, R., Owen, A. M., Doyon, J., & Fogel, S. M. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00507 · Cited by 68
“…where spindles are generally less frequent and smaller, such as elderly subjects (Martin et al., 2012), in clinical populations (Limoges et al., 2005; Steriade, 2005; Ferrarelli et al., 2007) or in noisy recordings, such as simultaneous EEG-fMRI, formal validation would also be required.”
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Tsanas, A., & Clifford, G. D. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00181 · Cited by 73
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 74
Sleep spindle and slow wave frequency reflect motor skill performance in primary school-age children
Astill, R. G., Piantoni, G., Raymann, R., Vis, J. C., Coppens, J. E., Walker, M. P., Stickgold, R., van der Werf, Y. D., & Someren, E. J. W. V. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00910 · Cited by 64
“…inspection of the performance of the automated algorithm indicated the need of slight adaptations in the parameter settings as compared to the settings used in Ferrarelli et al. (2007), in particular we used a lower threshold for spindle detection and we applied an additional smoothing window.”
MethodHigh Density Electroencephalography in Sleep Research: Potential, Problems, Future Perspective
Lustenberger, C., & Huber, R. (2012) · Frontiers in Neurology · doi:10.3389/fneur.2012.00077 · Cited by 66
“Many schizophrenic patients suffer from cognitive impairments (for a review see O’Carroll, 2000) that might be reflected in spindle deficits over the centroparietal cortex (Ferrarelli et al., 2007, 2010b).”
BackgroundMethodSelf-citationD-Cycloserine: An Evolving Role in Learning and Neuroplasticity in Schizophrenia
GOFF, D. C. (2012) · Schizophrenia Bulletin · doi:10.1093/schbul/sbs012 · Cited by 65
“Diminished density of sleep spindles has been linked to positive symptoms.(39) The impairment of 24-h delayed fear extinction recall demonstrated in schizophrenia subjects by Daphne Holt has also been observed in NR2C knockout mice(27) and can be produced by injection of an NMDA receptor blocker into medial ventral pr…”
The Contribution of Thalamocortical Core and Matrix Pathways to Sleep Spindles
Piantoni, G., Halgren, E., & Cash, S. S. (2016) · Neural Plasticity · doi:10.1155/2016/3024342 · Cited by 64
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“The relative inconsistency of reported results across studies that have examined sleep EEG findings in schizophrenia could be attributed to factors such as the size of the studies, patient heterogeneity and methodological limitations (Ferrarelli et al., 2007).”
ResultInfluentialSaletin, J., Goldstein‐Piekarski, A. N., Greer, S. M., Stark, S. M., Stark, C. E. L., & Walker, M. P. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3466-15.2016 · Cited by 59
Sleep correlates of cognition in early course psychotic disorders
Keshavan, M. S., Montrose, D. M., Miewald, J. M., & Jindal, R. D. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.05.027 · Cited by 62
“In a study of medicated schizophrenia patients, Ferrarelli et al. (2007, 2010) observed reduction in spindle activity.”
Adamczyk, M., Genzel, L., Dresler, M., Steiger, A., & Frieß, E. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00624 · Cited by 62
Sleep Spindles as an Electrographic Element: Description and Automatic Detection Methods
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Metzger, M. W., Walser, S. M., Dedic, N., Aprile-Garcia, F., Jakubcakova, V., Adamczyk, M., Webb, K. J., Uhr, M., Refojo, D., Schmidt, M. V., et al. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3487-16.2017 · Cited by 59
“…changes in either the number or the oscillation frequency of sleep spindles in several neuropsychiatric diseases and brain function in general (Ferrarelli et al., 2007; Lopez et al., 2010; Christensen et al., 2015; Nishida et al., 2016; Pótári et al., 2017), the observed slowing of spindle…”
BackgroundKikuma, K., Li, X., Perry, S., Li, Q., Goel, P., Chen, C., Kim, D., Stavropoulos, N., & Dickman, D. K. (2019) · Nature Communications · doi:10.1038/s41467-019-10992-6 · Cited by 53
Mander, B. A., Zhu, A. H., Lindquist, J. R., Villeneuve, S., Rao, V. R., Lu, B. S., Saletin, J., Ancoli‐Israel, S., Jagust, W. J., & Walker, M. P. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3033-16.2017 · Cited by 61
Obstructive sleep apnoea and schizophrenia — A research agenda
Kalucy, M. J., Grunstein, R., Lambert, T., & Glozier, N. (2013) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2012.10.003 · Cited by 55
Developmental changes in sleep spindle characteristics and sigma power across early childhood
McClain, I. J., Lustenberger, C., Achermann, P., Lassonde, J. M., Kurth, S., & LeBourgeois, M. K. (2016) · Neural Plasticity · doi:10.1155/2016/3670951 · Cited by 52
A Deep Learning Architecture to Detect Events in EEG Signals During Sleep
Chambon, S., Thorey, V., Arnal, P. J., Mignot, E. J.-M., & Gramfort, A. (2018) · Machine learning for signal processing ... · doi:10.1109/mlsp.2018.8517067 · Cited by 51
“The main difference between these lies in the thresholding part which is either performed on the rectified filtered signal [12], or on the instantaneous amplitude obtained after an Hilbert-Transform [11], on the root mean square of the filtered signal [10] or on the moving average of the rectified filtered signal [8].”
BackgroundMethodInfluentialIavarone, E., Simko, J., Shi, Y., Bertschy, M., García‐Amado, M., Litvak, P., Kaufmann, A.-K., O’Reilly, C., Amsalem, O., Abdellah, M., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112200 · Cited by 41
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Cortical regional differences of delta waves during all-night sleep in schizophrenia
Sekimoto, M., Kato, M., Watanabe, T., Kajimura, N., & Takahashi, K. (2010) · Schizophrenia Research · doi:10.1016/j.schres.2010.11.003 · Cited by 42
“To date, only a few reports on delta waves and spindles during sleep have been based on computer analysis (Hiatt et al., 1985; Ganguli et al., 1987; Keshavan et al., 1998; Ferrarelli et al., 2007).”
Thibaut, F., Boutros, N. N., Jarema, M., Oranje, B., Hasan, A., Daskalakis, Z. J., Wichniak, A., Schmitt, A., Riederer, P. F., Falkai, P., et al. (2015) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2015.1050061 · Cited by 43
“Diminished spindle activity was observed in chronic and antipsychotic-na ï ve early course schizophrenia patients, and in young nonpsychotic relatives of individuals with schizophrenia (Ferrarelli et al. 2007, Manoach at al.”
BackgroundSpindleU-Net: An Adaptive U-Net Framework for Sleep Spindle Detection in Single-Channel EEG
You, J., Jiang, D., Ma, Y., & Wang, Y. (2021) · IEEE Transactions on Neural Systems and Rehabilitation Engineering · doi:10.1109/tnsre.2021.3105443 · Cited by 42
The Munich vulnerability study on affective disorders: microstructure of sleep in high-risk subjects
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“Interestingly, a recent study using a 256-electrode high-density EEG during sleep also observed a spindle deficit in patients with schizophrenia when compared to patients with depression and healthy control subjects [17].”
Dickerson, D. D., & Bilkey, D. K. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00217 · Cited by 40
“, and Meyer, U. (2012). Schizophrenia: do all roads lead”
Nature and Nurture: Brain Region-Specific Inheritance of Sleep Neurophysiology in Adolescence
Rusterholz, T., Hamann, C., Markovic, A., Schmidt, S. J., Achermann, P., & Tarokh, L. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0945-18.2018 · Cited by 39
Non-rapid eye movement sleep and wake neurophysiology in schizophrenia
Kozhemiako, N., Wang, J., Jiang, C., Wang, L. A., Gai, G., Zou, K., Wang, Z., Yu, X., Zhou, L., Li, S., et al. (2022) · eLife · doi:10.7554/elife.76211 · Cited by 32
Self-citationThalamocortical dynamics of sleep: Roles of purinergic neuromodulation
Halassa, M. M. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.02.008 · Cited by 35
“This is consistent with findings that spindle density is greatly reduced in patients with schizophrenia, a disorder of sensory gating [38].”
ResultDiBa: A Data-Driven Bayesian Algorithm for Sleep Spindle Detection
Babadi, B., McKinney, S. M., Tarokh, V., & Ellenbogen, J. M. (2011) · IEEE Transactions on Biomedical Engineering · doi:10.1109/tbme.2011.2175225 · Cited by 37
Bartsch, U., Simpkin, A. J., Demanuele, C., Wamsley, E. J., Marston, H. M., & Jones, M. W. (2019) · Schizophrenia · doi:10.1038/s41537-019-0086-8 · Cited by 38
Sleep Spindles – As a Biomarker of Brain Function and Plasticity
Urakami, Y., Andreas, A., & George, K. (2012) · InTech eBooks · doi:10.5772/48427 · Cited by 43
“However, spindle activity of schizophrenic patients has reduced [117], and s positive relation between stage 2 spindle density and verbal declarative memory performance was observed [118].”
BackgroundMultichannel sleep spindle detection using sparse low-rank optimization
Parekh, A., Selesnick, I., Osorio, R. S., Varga, A. W., Rapoport, D. M., & Ayappa, I. A. (2017) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2017.06.004 · Cited by 35
Benson, K. L. (2008) · Sleep Medicine Clinics · doi:10.1016/j.jsmc.2008.01.001 · Cited by 33
Solano, A., Riquelme, L. A., Pérez-Chada, D., & Della‐Maggiore, V. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab360 · Cited by 33
Does abnormal non-rapid eye movement sleep impair declarative memory consolidation?
Lu, W., & Göder, R. (2011) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2011.08.001 · Cited by 33
Sleep spindle detection using time-frequency sparsity
Parekh, A., Selesnick, I., Rapoport, D. M., et al. (2014) · IEEE Signal Processing in Medicine and Biology Symposium · doi:10.1109/spmb.2014.7002965 · Cited by 30
“Except for the algorithm in [12](2), we implemented the remaining 5 detectors on the sleep spindle database.”
BackgroundMethodNon-REM sleep in major depressive disorder
Bovy, L., Weber, F. D., Tendolkar, I., Fernández, G., Czisch, M., Steiger, A., Zeising, M., & Dresler, M. (2022) · NeuroImage Clinical · doi:10.1016/j.nicl.2022.103275 · Cited by 33
Sleep-dependent memory consolidation and its implications for psychiatry
Goerke, M., Müller, N. G., & Cohrs, S. (2015) · Journal of Neural Transmission · doi:10.1007/s00702-015-1476-3 · Cited by 31
“However, studies using high-density EEG failed to confirm slow wave/delta deficits (Ferrarelli et al. 2007, 2010).”
ResultDonnelly, N. A., Bartsch, U., Moulding, H., Eaton, C. B., Marston, H. M., Hall, J. H., Hall, J., Owen, M. J., van den Bree, M. B. M., & Jones, M. W. (2022) · eLife · doi:10.7554/elife.75482 · Cited by 25
“Adult schizophrenia is consistently associated with reduced spindle activity (Ferrarelli et al., 2007; Ferrarelli et al., 2010; Lai et al., 2022), a finding replicated in a study of early onset schizophrenia (Gerstenberg et al.”
BackgroundResultInfluentialMahdavi, A., Qin, Y., Aubry, A.-S., Cornec, D., Kulikova, S. P., & Pinault, D. (2019) · Schizophrenia Research · doi:10.1016/j.schres.2020.04.029 · Cited by 27
Gonzalez, C. E., Jiang, X., Gonzalez-Martinez, J. A., & Halgren, E. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1786-21.2022 · Cited by 23
Sleep-related cognitive function and the K-complex in schizophrenia
Ramakrishnan, M., Sartory, G., van Beekum, A., Lohrmann, T., & Pietrowsky, R. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.06.019 · Cited by 23
Automated real‐time EEG sleep spindle detection for brain‐state‐dependent brain stimulation
Hassan, U., Feld, G. B., & Bergmann, T. O. (2022) · Journal of Sleep Research · doi:10.1111/jsr.13733 · Cited by 22
Corticothalamic gating of population auditory thalamocortical transmission in mouse
Ibrahim, B. A., Murphy, C. A., Muscioni, G., Taheri, A., Yudintsev, G., Kenyon, R. V., Berger-Wolf, T. Y., Banks, M. I., & Llano, D. A. (2021) · eLife · doi:10.7554/elife.56645 · Cited by 21
Sleep and Plasticity in Schizophrenia
Sprecher, K. E., Ferrarelli, F., & Benca, R. M. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_366 · Cited by 20
“…several spindle parameters compared to healthy controls, including power in the spindle range (13.75–15 Hz), spindle amplitude, duration, number, density (spindles/minute), and integrated spindle activity (ISA, calculated by integrating spindle activity over time) (Ferrarelli et al. 2007, 2010a).”
BackgroundInfluentialSelf-citationCannabis, psychosis and the thalamus: A theoretical review
Vukadinovic, Z., Herman, M., & Rosenzweig, I. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2013.02.013 · Cited by 18
Felice, A. D., Arcaro, C., Storti, S. F., Fiaschi, A., & Manganotti, P. (2013) · Clinical Neurophysiology · doi:10.1016/j.clinph.2013.06.002 · Cited by 17
“The counterpart of such data are observations of altered spindles density, amplitude and duration in conditions with defective cognition, such as schizophrenic patients (Ferrarelli et al., 2007), neurodegenerative diseases (Petit et al.”
BackgroundVisuomotor Adaptation Modulates the Clustering of Sleep Spindles Into Trains
Solano, A., Riquelme, L. A., Pérez-Chada, D., & Della‐Maggiore, V. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.803387 · Cited by 19
Is EEG a useful test in adult psychiatry?
Sand, T., Bjørk, M., & Vaaler, A. E. (2013) · Tidsskrift for Den norske legeforening · doi:10.4045/tidsskr.12.1253 · Cited by 14
“An increase in the amount of slow EEG activity in medicated and nonmedicated schizophrenia patients (36) may also be caused by drowsiness, as schizophrenia patients sleep less than healthy individuals (37) and have fewer sleep spindles (38).”
BackgroundBodien, Y. G., Tononi, G., & Postle, B. R. (2012) · Brain Connectivity · doi:10.1089/brain.2012.0100 · Cited by 14
“Additionally, sleep studies have repeatedly identified a decrease in sleep spindle measures in patients with schizophrenia (Ferrarelli et al., 2007; Ferrarelli et al., 2010; Vukadinovic, 2011; Wamsley et al., 2012).”
Self-citationAlizadeh, Z., Azimi, A., & Ghorbani, M. (2022) · The Journal of Neuroscience · doi:10.1523/jneurosci.2515-21.2022 · Cited by 14
The effect of typical and atypical antipsychotic drugs on sleep of schizophrenic patients
Winokur, A., & Kamath, J. (2008) · Birkhäuser Basel eBooks · doi:10.1007/978-3-7643-8561-3_24 · Cited by 14
The Dreaming Brain/Mind: A Role in Understanding Complex Mental Disorders?
D’Agostino, A., Limosani, I., & Scarone, S. (2012) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2012.00003 · Cited by 13
“In this regard, it seems interesting to note that sleep spindle density has been found to be reduced in schizophrenic subjects (Ferrarelli et al., 2007).”
BackgroundAutistic Traits Are Associated With Decreased Activity of Fast Sleep Spindles During Adolescence
Merikanto, I., Kuula, L., Makkonen, T., Salmela, L., Räikkönen, K., & Pesonen, A. (2019) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.7662 · Cited by 13
“As a limitation, although the method used in this study by Ferrarelli et al. 37,54 is widely applied, there is still lack of cross-validation studies across different sleep spindle analysis methods.”
Role of Sleep Spindles and Slow-Wave Activity in Integrating New Information in Semantic Memory
Tamminen, J., Ralph, M. A. L., & Lewis, P. A. (2013) · PsycEXTRA Dataset · doi:10.1037/e633262013-964 · Cited by 11
Sleep Consolidation Potentiates Sensorimotor Adaptation
Solano, A., Lerner, G., Griffa, G., Deleglise, Á., Caffaro, P., Riquelme, L. A., Pérez-Chada, D., & Della‐Maggiore, V. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0325-24.2024 · Cited by 9
Slow oscillation-spindle coupling predicts sequence-based language learningPreprint
Cross, Z. R., Helfrich, R. F., Corcoran, A. W., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.13.948539 · Cited by 10
Genetics, sleep and memory: a recall-by-genotype study of ZNF804A variants and sleep neurophysiology
Hellmich, C., Durant, C. F., Jones, M. W., Timpson, N. J., Bartsch, U., & Corbin, L. J. (2015) · BMC Medical Genetics · doi:10.1186/s12881-015-0244-4 · Cited by 10
“Spindle activity has also been shown to be reduced in patients with schizophrenia [37], and reduced spindle number and density correlated with impaired overnight improvement in a motor sequence task (MST) [38] (also in patients).”
BackgroundBOLD signatures of sleepPreprint
Song, C., Boly, M., Tagliazucchi, E., Laufs, H., & Tononi, G. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/531186 · Cited by 8
Self-citationCircadian Rhythms of Perineuronal Net CompositionPreprint
Pantazopoulos, H., Gisabella, B., Rexrode, L., Benefield, D., Yildiz, E., Seltzer, P., Valeri, J., Chelini, G., Reich, A., Ardelt, M., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.21.053751 · Cited by 9
Denis, D., Baran, B., Mylonas, D., Spitzer, C., Raymond, N., Talbot, C., Kohnke, E., Larson, O., Stickgold, R., Keshavan, M. S., et al. (2024) · Schizophrenia Research · doi:10.1016/j.schres.2024.10.026 · Cited by 8
Estimation of Time-Varying Spectral Peaks and Decomposition of EEG Spectrograms
Stokes, P. A., & Prerau, M. J. (2020) · IEEE Access · doi:10.1109/access.2020.3042737 · Cited by 7
“Alternatively, the EEG signal is bandpassed to the frequency range of interest and instantaneous amplitude or power within the band computed [18], [24], [27], [31], [38], e.g., via Hilbert transform.”
BackgroundMethodSchizophrenia as a disturbance of cortical sensory maps
Vukadinovic, Z. (2012) · Translational Neuroscience · doi:10.2478/s13380-012-0043-8 · Cited by 7
Sleep, memory and schizophrenia
Manoach, D. S., & Stickgold, R. (2015) · Sleep Medicine · doi:10.1016/j.sleep.2015.01.009 · Cited by 7
Bedtime to the brain: How infants sleep habits intertwine with sleep neurophysiologyPreprint
Schoch, S. F., Jaramillo, V., Markovic, A., Huber, R., Kohler, M., Jenni, O. G., Lustenberger, C., & Kurth, S. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.08.467800 · Cited by 7
Self-citationDimitriades, M. E., Osorio-Forero, A., Fattinger, S., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.06.620875 · Cited by 6
Self-citation
Metadata
- Authors
- Ferrarelli, F., Huber, R., Peterson, M. J., Massimini, M., Murphy, M., Riedner, B. A., Watson, A., Bria, P., & Tononi, G.
- Affiliations
- University of Wisconsin–Madison (US)
- Don Carlo Gnocchi Foundation (IT)
- Venue
- American Journal of Psychiatry
- Published
- 2007-03
- Volume
- 164
- Issue
- 3
- Pages
- 483-492
- ISSN
- 0002-953X (ISSN-L)
- 1535-7228
- OpenAlex
- W2077633827
- Cited by
- 541
- References
- 49
- Citations by year
- 2026: 28 · 2025: 32 · 2024: 32 · 2023: 21 · 2022: 39 · 2021: 29 · 2020: 42 · 2019: 31 · 2018: 32 · 2017: 39 · 2016: 39 · 2015: 39 · 2014: 28 · 2013: 32 · 2012: 21
- FWCI
- 7.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- schizophrenia, sleep spindles, high-density EEG, sleep rhythm, thalamic reticular nucleus, thalamocortical connections, corticothalamic connections, depression, biomarkers, EEG power spectra
- MeSH terms
- Adolescent, Adult, Brain Mapping, Cerebral Cortex, Depressive Disorder, Diagnosis, Differential, Electroencephalography, Female, Humans, Male, Middle Aged, Neural Pathways, Parietal Lobe, Reticular Formation, Schizophrenia, Sleep, Sleep Stages, Thalamus, Biomarkers
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