Sleep-dependent memory consolidation in schizophrenia: A systematic review and meta-analysis

Demirlek, Cemal; Bora, Emre

doi:10.1016/j.schres.2023.02.028

Cited by 5 publications

(6 citation statements)

References 61 publications

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“…With regard to MST performance, although we replicated prior findings of impaired sleepdependent memory consolidation in SCZ (Demanuele et al, 2017;Demirlek and Bora, 2023), previous reports linking overnight MST improvement and spindle density (Mylonas et al, 2020a;Wamsley et al, 2012) were not supported by the current study. Future work will be needed to resolve these apparent discrepancies, whether they reflect purely statistical (type I or type II) errors, or systematic differences in factors such as sample composition, demographics, medication regimens or inpatient versus outpatient settings.…”

Section: Discussioncontrasting

confidence: 93%

A spectrum of altered non-rapid eye movement sleep in schizophrenia

Kozhemiako,

Jiang,

Sun

et al. 2023

Preprint

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Background: Multiple facets of sleep neurophysiology, including electroencephalography (EEG) metrics such as non-rapid eye movement (NREM) spindles and slow oscillations (SO), are altered in individuals with schizophrenia (SCZ). However, beyond group-level analyses which treat all patients as a unitary set, the extent to which NREM deficits vary among patients is unclear, as are their relationships to other sources of heterogeneity including clinical factors, illness duration and ageing, cognitive profiles and medication regimens. Using newly collected high density sleep EEG data on 103 individuals with SCZ and 68 controls, we first sought to replicate our previously reported (Kozhemiako et. al, 2022) group-level mean differences between patients and controls (original N=130). Then in the combined sample (N=301 including 175 patients), we characterized patient-to-patient variability in NREM neurophysiology. Results: We replicated all group-level mean differences and confirmed the high accuracy of our predictive model (Area Under the ROC Curve, AUC = 0.93 for diagnosis). Compared to controls, patients showed significantly increased between-individual variability across many (26%) sleep metrics, with patterns only partially recapitulating those for group-level mean differences. Although multiple clinical and cognitive factors were associated with NREM metrics including spindle density, collectively they did not account for much of the general increase in patient-to-patient variability. Medication regimen was a greater (albeit still partial) contributor to variability, although original group mean differences persisted after controlling for medications. Some sleep metrics including fast spindle density showed exaggerated age-related effects in SCZ, and patients exhibited older predicted biological ages based on an independent model of ageing and the sleep EEG. Conclusion: We demonstrated robust and replicable alterations in sleep neurophysiology in individuals with SCZ and highlighted distinct patterns of effects contrasting between-group means versus within-group variances. We further documented and controlled for a major effect of medication use, and pointed to greater age-related change in NREM sleep in patients. That increased NREM heterogeneity was not explained by standard clinical or cognitive patient assessments suggests the sleep EEG provides novel, nonredundant information to support the goals of personalized medicine. Collectively, our results point to a spectrum of NREM sleep deficits among SCZ patients that can be measured objectively and at scale, and that may offer a unique window on the etiological and genetic diversity that underlies SCZ risk, treatment response and prognosis.

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Section: Discussioncontrasting

confidence: 93%

A spectrum of altered non-rapid eye movement sleep in schizophrenia

Kozhemiako,

Jiang,

Sun

et al. 2023

Preprint

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“…We examined sleep oscillations in relation to sleep-dependent memory consolidation in early-course minimally medicated psychosis patients and young, non-psychotic first-degree relatives. Replicating previous work, and extending it to early course patients with schizophrenia, we found pronounced deficits in sleep spindle density and overnight procedural memory consolidation patients relative to controls (Demirlek & Bora, 2023; Lai et al, 2021). However, neither of these deficits extended to early course patients with other psychoses or non-psychotic first-degree relatives.…”

Section: Discussionsupporting

confidence: 86%

“…Sleep spindles are propagated to the cortex, where they induce long-term potentiation (LTP) and synaptic plasticity, facilitating overnight memory consolidation (Peyrache & Seibt, 2020; Rosanova & Ulrich, 2005; Seibt et al, 2017; Steriade & Timofeev, 2003; Werk et al, 2005). Chronic patients with schizophrenia have reduced sleep-dependent procedural and declarative memory consolidation (Baran et al, 2018; Göder et al, 2015; Manoach et al, 2004; see Demirlek & Bora, 2023 for meta-analysis) that correlates with spindle and slow oscillation (SO)-spindle coupling deficits (Göder et al, 2015; Manoach et al, 2010; Wamsley et al, 2012). In young, early course antipsychotic-naïve schizophrenia patients and non-psychotic first-degree relatives, sleep-dependent memory consolidation has not been examined, but spindle deficits correlate with more general cognitive impairments (Manoach et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…The copyright holder for this this version posted November 2, 2023. ; https://doi.org/10. 1101/2023 disorders in either early course (Manoach et al, 2014) or chronic (Ferrarelli & Tononi, 2017) samples. These findings suggest that the sleep spindle deficit in schizophrenia is an endophenotype reflecting genetic risk for schizophrenia (Manoach et al, 2016;Schilling et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

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NREM sleep oscillations and their relations with sleep-dependent memory consolidation in early course psychosis and first-degree relatives

Denis,

Baran,

Mylonas

et al. 2023

Preprint

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Sleep spindles are believed to mediate sleep-dependent memory consolidation, particularly when coupled to neocortical slow oscillations. Schizophrenia is characterized by a deficit in sleep spindles that correlates with reduced overnight memory consolidation. Here, we examined sleep spindle activity, slow oscillation-spindle coupling, and both motor procedural and verbal declarative memory consolidation in early course, minimally medicated psychosis patients and non-psychotic first-degree relatives. Using a four-night experimental procedure, we observed significant deficits in spindle density and amplitude in patients relative to controls that were driven by individuals with schizophrenia. Schizophrenia patients also showed reduced sleep-dependent consolidation of motor procedural memory, which correlated with spindle density. Contrary to expectations, there were no group differences in the consolidation of declarative memory on a word pairs task. Nor did the relatives of patients differ in spindle activity or memory consolidation compared with controls, however increased consistency in the timing of SO-spindle coupling were seen in both patient and relatives. Our results extend prior work by demonstrating correlated deficits in sleep spindles and sleep-dependent motor procedural memory consolidation in early course, minimally medicated patients with schizophrenia, but not in first-degree relatives. This is consistent with other work in suggesting that impaired sleep-dependent memory consolidation has some specificity for schizophrenia and is a core feature rather than reflecting the effects of medication or chronicity.Statement of significanceWe investigated sleep neurophysiology and memory consolidation in minimally-medicated, early course psychosis patients and unaffected first-degree relatives of patients in a four-night study. Early-course schizophrenia patients had a sleep spindle deficit that correlated with reduced procedural memory consolidation. Although first-degree relatives did not show any deficit in spindles or memory consolidation, the spindles of both relatives and patients showed increased consistency of the temporal coupling of spindles with slow oscillations compared with controls. These results suggest that sleep spindle and memory consolidation deficits are a core feature of schizophrenia. Spindle deficits may be a biomarker of schizophrenia modifiable by treatment, and motivate the development of targeted novel interventions.

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“…Sleep disorder is the most common symptom experienced by patients with schizophrenia, with 30%-80% of patients experiencing sleep disorders. A study conducted on outpatient patients with schizophrenia showed that 44% of patients have insomnia symptoms [14,15]. Sleep disorders can lead to a decrease in the quality of life and cognitive impairment in patients with schizophrenia.…”

Section: Introductionmentioning

confidence: 99%

The relationship between sleep disorders and aggressive behaviour among schizophrenia patients in the community: A moderated mesomeric effect model

Ye,

Wu,

Yue

et al. 2023

Preprint

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Objective Sleep disorder is the most common complaint of patients with schizophrenia, which can not only lead to poor prognosis and low survival rate but also aggressive behaviour, posing a significant threat to social security and stability. The aim of this study is to explore the mediating role of depression in the relationship between sleep disorders and aggressive behaviour in people with schizophrenia living in the community, as well as the regulatory role of family intimacy and adaptability. These findings, in turn, may provide a theoretical basis and constructive suggestions for resolving the physical and mental health problems of these patients.Method A convenience sampling method was used to select schizophrenia patients from Pengzhou City, China, for follow-up, and a survey was conducted on the Questionnaire Star platform. The survey included questions about general demographic data and disease-related questionnaires: the Pittsburgh Sleep Quality Index (PSQI), the Modified Over Aggression Scale (MOAS) revised Chinese version, the Self-Rating Depression Scale (SDS), and the Family Adaptability and Cohesion Scale, Second Edition. FACES-II and SPSS 21.0 were used to organize and analyse the data.Results A total of 818 schizophrenia patients living in the community participated in the survey, and 785 valid questionnaires were ultimately collected for a response rate of 95.97%. The results of multivariate analysis indicate that gender, psychiatric medication use, outpatient follow-up, and sleep disorders are the factors influencing aggressive behaviour. Depression played a partial mediating role between sleep disorders and aggressive behaviour, and the indirect effect size value was 0.043 (57.33% of the total). Sleep disorders and family intimacy (β=-0.009, P < 0.01) and adaptability (β=-0.145, P < 0.001) can significantly predict depression.Conclusion 1. The incidence of aggressive behaviour and sleep disorders in patients with schizophrenia living in the community is low. 2. Depression plays a partial mediating role in the relationship between sleep disorders and aggressive behaviour. 3. Family intimacy and adaptability play a regulatory role between depression and sleep disorders.

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Sleep-dependent memory consolidation in schizophrenia: A systematic review and meta-analysis

Cited by 5 publications

References 61 publications

A spectrum of altered non-rapid eye movement sleep in schizophrenia

A spectrum of altered non-rapid eye movement sleep in schizophrenia

NREM sleep oscillations and their relations with sleep-dependent memory consolidation in early course psychosis and first-degree relatives

The relationship between sleep disorders and aggressive behaviour among schizophrenia patients in the community: A moderated mesomeric effect model

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