Distributed slow-wave dynamics during sleep predict memory consolidation and its impairment in schizophrenia

Abstract The slow waves (SW) of non-rapid eye movement (NREM) sleep reflect neocortical components of network activity during sleep-dependent information processing; their disruption may therefore impair memory consolidation. Here, we quantify sleep-dependent consolidation of motor sequence memory, alongside sleep EEG-derived SW properties and synchronisation, and SW–spindle coupling in 21 patients suffering from schizophrenia and 19 healthy volunteers. Impaired memory consolidation in patients culminated in an overnight improvement in motor sequence task performance of only 1.6%, compared with 15% in controls. During sleep after learning, SW amplitudes and densities were comparable in healthy controls and patients. However, healthy controls showed a significant 45% increase in frontal-to-occipital SW coherence during sleep after motor learning in comparison with a baseline night (baseline: 0.22 ± 0.05, learning: 0.32 ± 0.05); patient EEG failed to show this increase (baseline: 0.22 ± 0.04, learning: 0.19 ± 0.04). The experience-dependent nesting of spindles in SW was similarly disrupted in patients: frontal-to-occipital SW–spindle phase-amplitude coupling (PAC) significantly increased after learning in healthy controls (modulation index baseline: 0.17 ± 0.02, learning: 0.22 ± 0.02) but not in patients (baseline: 0.13 ± 0.02, learning: 0.14 ± 0.02). Partial least-squares regression modelling of coherence and PAC data from all electrode pairs confirmed distributed SW coherence and SW–spindle coordination as superior predictors of overnight memory consolidation in healthy controls but not in patients. Quantifying the full repertoire of NREM EEG oscillations and their long-range covariance therefore presents learning-dependent changes in distributed SW and spindle coordination as fingerprints of impaired cognition in schizophrenia.

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Neurophysiological predictors of memory impairment in schizophrenia: decoupled slow-wave dynamics during non-REM sleep

10.1101/578039 ◽

2019 ◽

Author(s):

Ullrich Bartsch ◽

Andrew Simpkin ◽

Charmaine Demanuele ◽

Erin Wamsley ◽

Hugh Marston ◽

...

Keyword(s):

Healthy Volunteers ◽

Long Range ◽

Memory Consolidation ◽

Network Activity ◽

Rapid Eye Movement Sleep ◽

Least Squares Regression ◽

Motor Sequence ◽

Wave Dynamics ◽

Sequence Memory ◽

Phase Amplitude

AbstractThe slow-waves (SW) of non-rapid eye movement sleep (NREM) reflect neocortical components of network activity during sleep-dependent information processing; their disruption may therefore contribute to impaired memory consolidation. Here, we quantify SW dynamics relative to motor sequence memory in patients suffering schizophrenia and healthy volunteers.Patients showed normal intrinsic SW properties but impaired SW coherence, which failed to exhibit the learning-dependent increases evident in healthy volunteers. SW-spindle phase amplitude coupling across distributed EEG electrodes was also dissociated from experience in patients, with long-range fronto-parietal and -occipital networks most severely affected. Partial least squares regression modelling confirmed distributed SW coherence and SW-spindle coordination as predictors of overnight memory consolidation in healthy controls, but not in patients.Quantifying the full repertoire of NREM EEG oscillations and their long-range covariance therefore presents learning-dependent changes in distributed SW and spindle coordination as fingerprints of impaired cognition in schizophrenia.

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Schizophrenia-associated variation at ZNF804A correlates with altered experience-dependent dynamics of sleep slow waves and spindles in healthy young adults

SLEEP ◽

10.1093/sleep/zsab191 ◽

2021 ◽

Author(s):

Ullrich Bartsch ◽

Laura J Corbin ◽

Charlotte Hellmich ◽

Michelle Taylor ◽

Kayleigh E Easey ◽

...

Keyword(s):

Memory Consolidation ◽

Neural Circuit ◽

Activity Patterns ◽

Nrem Sleep ◽

Network Activity ◽

Healthy Population ◽

Adult Males ◽

Motor Sequence ◽

Performance Improvements ◽

Common Genetic Variants

Abstract The rs1344706 polymorphism in ZNF804A is robustly associated with schizophrenia and schizophrenia is, in turn, associated with abnormal non-rapid eye movement (NREM) sleep neurophysiology. To examine whether rs1344706 is associated with intermediate neurophysiological traits in the absence of disease, we assessed the relationship between genotype, sleep neurophysiology, and sleep-dependent memory consolidation in healthy participants. We recruited healthy adult males with no history of psychiatric disorder from the Avon Longitudinal Study of Parents and Children (ALSPAC) birth cohort. Participants were homozygous for either the schizophrenia-associated ‘A’ allele (N=22) or the alternative ‘C’ allele (N=18) at rs1344706. Actigraphy, polysomnography (PSG) and a motor sequence task (MST) were used to characterize daily activity patterns, sleep neurophysiology and sleep-dependent memory consolidation. Average MST learning and sleep-dependent performance improvements were similar across genotype groups, albeit more variable in the AA group. During sleep after learning, CC participants showed increased slow-wave (SW) and spindle amplitudes, plus augmented coupling of SW activity across recording electrodes. SW and spindles in those with the AA genotype were insensitive to learning, whilst SW coherence decreased following MST training. Accordingly, NREM neurophysiology robustly predicted the degree of overnight motor memory consolidation in CC carriers, but not in AA carriers. We describe evidence that rs1344706 polymorphism in ZNF804A is associated with changes in the coordinated neural network activity that supports offline information processing during sleep in a healthy population. These findings highlight the utility of sleep neurophysiology in mapping the impacts of schizophrenia-associated common genetic variants on neural circuit oscillations and function.

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0112 Sleep-Dependent Motor Sequence Memory Consolidation in Individuals with Periodic Limb Movements

SLEEP ◽

10.1093/sleep/zsy061.111 ◽

2018 ◽

Vol 41 (suppl_1) ◽

pp. A44-A44

Author(s):

L B Ray ◽

V Sergeeva ◽

J Viczko ◽

A M Owen ◽

S M Fogel

Keyword(s):

Memory Consolidation ◽

Periodic Limb Movements ◽

Motor Sequence ◽

Limb Movements ◽

Sequence Memory

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The effect of 12-week physical exercise intervention to the sleep-dependent motor sequence memory consolidation in schizophrenia

10.5353/th_991044104149303414 ◽

2017 ◽

Author(s):

Lik-hang, Lincoln Lo

Keyword(s):

Physical Exercise ◽

Memory Consolidation ◽

Exercise Intervention ◽

Motor Sequence ◽

Sequence Memory

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Schizophrenia-associated variation at ZNF804A correlates with altered experience-dependent dynamics of sleep slow-waves and spindles in healthy young adults

10.1101/2020.05.01.072165 ◽

2020 ◽

Author(s):

Ullrich Bartsch ◽

Laura J Corbin ◽

Charlotte Hellmich ◽

Michelle Taylor ◽

Kayleigh E Easey ◽

...

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Neural Circuit ◽

Activity Patterns ◽

Nrem Sleep ◽

Slow Waves ◽

Network Activity ◽

Healthy Population ◽

Adult Males ◽

Performance Improvements

ABSTRACTBackgroundThe rs1344706 polymorphism in ZNF804A is robustly associated with schizophrenia (SZ), yet brain and behavioral phenotypes related to this variant have not been extensively characterized. In turn, SZ is associated with abnormal non-rapid eye movement (NREM) sleep neurophysiology. To examine whether rs1344706 is associated with intermediate neurophysiological traits in the absence of disease, we assessed the relationship between genotype, sleep neurophysiology, and sleep-dependent memory consolidation in healthy participants.MethodsWe recruited healthy adult males, with no history of psychiatric disorder, from the Avon Longitudinal Study of Parents and Children (ALSPAC) birth cohort. Participants were homozygous for either the SZ-associated ‘A’ allele (N=25) or the alternative ‘C’ allele (N=22) at rs1344706. Actigraphy, polysomnography (PSG) and a motor sequencing task (MST) were used to characterize daily activity patterns, sleep neurophysiology and sleep-dependent memory consolidation.ResultsAverage MST learning and sleep-dependent performance improvements were similar across genotype groups, but with increased variability in the AA group. CC participants showed increased slow-wave and spindle amplitudes, plus augmented coupling of slow-wave activity across recording electrodes after learning. Slow-waves and spindles in those with the AA genotype were insensitive to learning, whilst slow-wave coherence decreased following MST training.ConclusionWe describe evidence that rs1344706 polymorphism in ZNF804A is associated with changes in experience- and sleep-dependent, local and distributed neural network activity that supports offline information processing during sleep in a healthy population. These findings highlight the utility of sleep neurophysiology in mapping the impacts of SZ-associated variants on neural circuit oscillations and function.

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Sleep-dependent motor sequence memory consolidation in individuals with periodic limb movements

Sleep Medicine ◽

10.1016/j.sleep.2017.11.810 ◽

2017 ◽

Vol 40 ◽

pp. e276

Author(s):

L.B. Ray ◽

V. Sergeeva ◽

J. Viczko ◽

A.M. Owen ◽

S.M. Fogel

Keyword(s):

Memory Consolidation ◽

Periodic Limb Movements ◽

Motor Sequence ◽

Limb Movements ◽

Sequence Memory

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Sleep Increases Amplitude of Mu-Beta Oscillations during Motor Sequence Memory Consolidation

NeuroImage ◽

10.1016/s1053-8119(09)70189-2 ◽

2009 ◽

Vol 47 ◽

pp. S55

Author(s):

G. Albouy ◽

F. Lecaignard ◽

C. Delpuech ◽

P.E. Aguera ◽

P.H. Luppi ◽

...

Keyword(s):

Memory Consolidation ◽

Motor Sequence ◽

Beta Oscillations ◽

Sequence Memory

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Non-REM sleep facilitates consolidation of contextual fear memory through temporal coding among hippocampal neurons

10.1101/2020.05.29.123356 ◽

2020 ◽

Author(s):

Quinton M. Skilling ◽

Brittany C. Clawson ◽

Bolaji Eniwaye ◽

James Shaver ◽

Nicolette Ognjanovski ◽

...

Keyword(s):

Memory Consolidation ◽

Hippocampal Neurons ◽

Critical Role ◽

Nrem Sleep ◽

Spike Timing ◽

Temporal Coding ◽

Network Activity ◽

Prior Learning ◽

Information Encoding

SummarySleep plays a critical role in memory consolidation, although the exact mechanisms mediating this process are unknown. Combining computational and in vivo experimental approaches, we test the hypothesis that reduced cholinergic input to the hippocampus during non-rapid eye movement (NREM) sleep generates stable spike timing relationships between neurons. We find that the order of firing among neurons during a period of NREM sleep reflects their relative firing rates during prior wake, and changes as a function of prior learning. We show that learning-dependent pattern formation (e.g. “replay”) in the hippocampus during NREM, together with spike timing dependent plasticity (STDP), restructures network activity in a manner similar to that observed in brain circuits across periods of sleep. This suggests that sleep actively promotes memory consolidation by switching the network from rate-based to firing phase-based information encoding.

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