scholarly journals Cueing memory during sleep is optimal during slow-oscillatory up-states

2017 ◽  
Author(s):  
Maurice Göldi ◽  
Eva van Poppel ◽  
Björn Rasch ◽  
Thomas Schreiner

AbstractSlow oscillations play a major role in neural plasticity. It is assumed that slow oscillatory up-states represent crucial time windows for memory reactivation and consolidation during sleep. Here we experimentally tested this assumption by utilizing closed-loop targeted memory reactivation (closed-loop TMR): Healthy participants were re-exposed to prior learned foreign vocabulary during up- and down-states of slow oscillations, respectively, in a within-subject design. We show that presenting memory cues during slow oscillatory up-states robustly improves recall performance, whereas memory cueing during down-states did not result in a clear behavioral benefit. On a neural basis successful memory reactivation during up-states was associated with a characteristic power increase in the theta and sleep spindle band. Such increases were completely absent for down-state memory cues. Our findings provide experimental support for the assumption that slow oscillatory up-states represent privileged time windows for memory reactivation, while the interplay of slow oscillations, theta and sleep spindle activity promote successful memory consolidation during sleep.

SLEEP ◽  
2020 ◽  
Vol 43 (12) ◽  
Author(s):  
Jules Schneider ◽  
Penelope A Lewis ◽  
Dominik Koester ◽  
Jan Born ◽  
Hong-Viet V Ngo

Abstract Study Objectives Cortical slow oscillations (SOs) and thalamocortical sleep spindles hallmark slow wave sleep and facilitate memory consolidation, both of which are reduced with age. Experiments utilizing auditory closed-loop stimulation to enhance these oscillations showed great potential in young and older subjects. However, the magnitude of responses has yet to be compared between these age groups. We examined the possibility of enhancing SOs and performance on different memory tasks in a healthy middle-aged population using this stimulation and contrast effects to younger adults. Methods In a within-subject design, 17 subjects (55.7 ± 1.0 years) received auditory stimulation in synchrony with SO up-states, which was compared to a no-stimulation sham condition. Overnight memory consolidation was assessed for declarative word-pairs and procedural finger-tapping skill. Post-sleep encoding capabilities were tested with a picture recognition task. Electrophysiological effects of stimulation were compared to a previous younger cohort (n = 11, 24.2 ± 0.9 years). Results Overnight retention and post-sleep encoding performance of the older cohort revealed no beneficial effect of stimulation, which contrasts with the enhancing effect the same stimulation protocol had in our younger cohort. Auditory stimulation prolonged endogenous SO trains and induced sleep spindles phase-locked to SO up-states in the older population. However, responses were markedly reduced compared to younger subjects. Additionally, the temporal dynamics of stimulation effects on SOs and spindles differed between age groups. Conclusions Our findings suggest that the susceptibility to auditory stimulation during sleep drastically changes with age and reveal the difficulties of translating a functional protocol from younger to older populations.


Author(s):  
Jules Schneider ◽  
Penelope A. Lewis ◽  
Dominik Koester ◽  
Jan Born ◽  
Hong-Viet V. Ngo

AbstractBackgroundCortical slow oscillations (SOs) and thalamo-cortical sleep spindles hallmark slow wave sleep and facilitate sleep-dependent memory consolidation. Experiments utilising auditory closed-loop stimulation to enhance these oscillations have shown great potential in young and older subjects. However, the magnitude of responses has yet to be compared between these age groups.ObjectiveWe examined the possibility of enhancing SOs and performance on different memory tasks in a healthy older population using auditory closed-loop stimulation and contrast effects to a young adult cohort.MethodsIn a within-subject design, subjects (n = 17, 55.7 ± 1.0 years, 9 female) received auditory click stimulation in synchrony with SO up-states, which was compared to a no-stimulation sham condition. Overnight memory consolidation was assessed for declarative word-pairs and procedural finger-tapping skill. Post-sleep encoding capabilities were tested with a picture recognition task. Electrophysiological effects of stimulation were compared to those reported previously in a younger cohort (n = 11, 24.2 ± 0.9 years, 8 female).ResultsOvernight retention and post-sleep encoding performance of the older cohort revealed no beneficial effect of stimulation, which contrasts with the enhancing effect the same stimulation protocol had in our younger cohort. Auditory stimulation prolonged endogenous SO trains and induced sleep spindles phase-locked to SO up-states in the older population. However, responses were markedly reduced compared to younger subjects. Additionally, the temporal dynamics of stimulation effects on SOs and spindles differed between age groups.ConclusionsOur findings suggest that the susceptibility to auditory stimulation during sleep drastically changes with age and reveal the difficulties of translating a functional protocol from younger to older populations.HighlightsAuditory closed-loop stimulation induced SOs and sleep spindles in older subjectsStimulation effects were reduced and overall susceptibility diminished with ageSlow oscillation and sleep spindle dynamics deviated from those in younger subjectsStimulation shows no evidence for memory effect in older subjects


2016 ◽  
Vol 22 (2) ◽  
pp. 164-179 ◽  
Author(s):  
Maki S. Koyama ◽  
Adriana Di Martino ◽  
Francisco X. Castellanos ◽  
Erica J. Ho ◽  
Enitan Marcelle ◽  
...  

AbstractObjectives: Clinical neuroscience is increasingly turning to imaging the human brain for answers to a range of questions and challenges. To date, the majority of studies have focused on the neural basis of current psychiatric symptoms, which can facilitate the identification of neurobiological markers for diagnosis. However, the increasing availability and feasibility of using imaging modalities, such as diffusion imaging and resting-state fMRI, enable longitudinal mapping of brain development. This shift in the field is opening the possibility of identifying predictive markers of risk or prognosis, and also represents a critical missing element for efforts to promote personalized or individualized medicine in psychiatry (i.e., stratified psychiatry). Methods: The present work provides a selective review of potentially high-yield populations for longitudinal examination with MRI, based upon our understanding of risk from epidemiologic studies and initial MRI findings. Results: Our discussion is organized into three topic areas: (1) practical considerations for establishing temporal precedence in psychiatric research; (2) readiness of the field for conducting longitudinal MRI, particularly for neurodevelopmental questions; and (3) illustrations of high-yield populations and time windows for examination that can be used to rapidly generate meaningful and useful data. Particular emphasis is placed on the implementation of time-appropriate, developmentally informed longitudinal designs, capable of facilitating the identification of biomarkers predictive of risk and prognosis. Conclusions: Strategic longitudinal examination of the brain at-risk has the potential to bring the concepts of early intervention and prevention to psychiatry. (JINS, 2016, 22, 164–179)


2021 ◽  
Author(s):  
Felipe A. Torres ◽  
Patricio Orio ◽  
María-José Escobar

AbstractSlow-wave sleep cortical brain activity, conformed by slow-oscillations and sleep spindles, plays a key role in memory consolidation. The increase of the power of the slow-wave events, obtained by auditory sensory stimulation, positively correlates to memory consolidation performance. However, little is known about the experimental protocol maximizing this effect, which could be induced by the power of slow-oscillation, the number of sleep spindles, or the timing of both events’ co-occurrence. Using a mean-field model of thalamocortical activity, we studied the effect of several stimulation protocols, varying the pulse shape, duration, amplitude, and frequency, as well as a target-phase using a closed-loop approach. We evaluated the effect of these parameters on slow-oscillations (SO) and sleep-spindles (SP), considering: (i) the power at the frequency bands of interest, (ii) the number of SO and SP, (iii) co-occurrences between SO and SP, and (iv) synchronization of SP with the up-peak of the SO. The first three targets are maximized using a decreasing ramp pulse with a pulse duration of 50 ms. Also, we observed a reduction in the number of SO when increasing the stimulus energy by rising its amplitude. To assess the target-phase parameter, we applied closed-loop stimulation at 0º, 45º, and 90º of the phase of the narrow-band filtered ongoing activity, at 0.85 Hz as central frequency. The 0º stimulation produces better results in the power and number of SO and SP than the rhythmic or aleatory stimulation. On the other hand, stimulating at 45º or 90º change the timing distribution of spindles centers but with fewer co-occurrences than rhythmic and 0º phase. Finally, we propose the application of closed-loop stimulation at the rising zero-cross point using pulses with a decreasing ramp shape and 50 ms of duration for future experimental work.Author summaryDuring the non-REM (NREM) phase of sleep, events that are known as slow oscillations (SO) and spindles (SP) can be detected by EEG. These events have been associated with the consolidation of declarative memories and learning. Thus, there is an ongoing interest in promoting them during sleep by non-invasive manipulations such as sensory stimulation. In this paper, we used a computational model of brain activity that generates SO and SP, to investigate which type of sensory stimulus –shape, amplitude, duration, periodicity– would be optimal for increasing the events’ frequency and their co-occurrence. We found that a decreasing ramp of 50 ms duration is the most effective. The effectiveness increases when the stimulus pulse is delivered in a closed-loop configuration triggering the pulse at a target phase of the ongoing SO activity. A desirable secondary effect is to promote SPs at the rising phase of the SO oscillation.


2010 ◽  
Vol 104 (6) ◽  
pp. 3433-3438 ◽  
Author(s):  
Francois Windels ◽  
James W. Crane ◽  
Pankaj Sah

Slow oscillations (<1 Hz) in neural activity occur during sleep and quiet wakefulness in both animals and humans. Single-cell recordings in cortical neurons have shown that these oscillations are driven by a combination of excitatory and inhibitory synaptic inputs. During up-states, although the ratio between them varies between cells, excitation and inhibition follow similar time courses. Neurons in the basolateral amygdala (BLA) also show slow oscillations between the resting membrane potential (down-state) and depolarized potentials (up-states). Delivery of footshock during the down-state fully reproduces up-states in these cells. Here we report that up-states in BLA principal neurons up-states begin with an excitatory drive that is rapidly (within ∼50 ms) overwhelmed by inhibitory input. This excess of inhibitory drive is short lasting (300–400 ms), after which up-states are maintained by a tight balance between excitation and inhibition. This initial large inhibitory input restricts action potential generation and reduces the firing frequency of these cells. These results indicate that, in contrast to cortical neurons, up-states in BLA neurons show an initial period of strong cortically driven feed-forward inhibition. For the remainder of the up-state, feedback inhibition then acts to balance excitatory input.


2015 ◽  
Vol 35 (17) ◽  
pp. 6630-6638 ◽  
Author(s):  
H.-V. V. Ngo ◽  
A. Miedema ◽  
I. Faude ◽  
T. Martinetz ◽  
M. Molle ◽  
...  

2014 ◽  
Vol 61 (7) ◽  
pp. 2092-2101 ◽  
Author(s):  
Ren Xu ◽  
Ning Jiang ◽  
Natalie Mrachacz-Kersting ◽  
Chuang Lin ◽  
Guillermo Asin Prieto ◽  
...  

2020 ◽  
Author(s):  
Thomas Schreiner ◽  
Marit Petzka ◽  
Tobias Staudigl ◽  
Bernhard P. Staresina

ABSTRACTSleep is thought to support memory consolidation via reactivation of prior experiences, with particular electrophysiological sleep signatures (slow oscillations (SOs) and sleep spindles) gating the information flow between relevant brain areas. However, empirical evidence for a role of endogenous memory reactivation (i.e., without experimentally delivered memory cues) for consolidation in humans is lacking. Here, we devised a paradigm in which participants acquired associative memories before taking a nap. Multivariate decoding was then used to capture endogenous memory reactivation during non-rapid eye movement (NREM) sleep. Results revealed reactivation of learning material during SO-spindle complexes, with the precision of SO-spindle coupling predicting reactivation strength. Critically, reactivation strength in turn predicted the level of consolidation across participants. These results elucidate the memory function of sleep in humans and emphasize the importance of SOs and spindles in clocking endogenous consolidation processes.


2020 ◽  
Vol 375 (1799) ◽  
pp. 20190227 ◽  
Author(s):  
Masami Tatsuno ◽  
Soroush Malek ◽  
LeAnna Kalvi ◽  
Adrian Ponce-Alvarez ◽  
Karim Ali ◽  
...  

Interaction between hippocampal sharp-wave ripples (SWRs) and UP states, possibly by coordinated reactivation of memory traces, is conjectured to play an important role in memory consolidation. Recently, it was reported that SWRs were differentiated into multiple subtypes. However, whether cortical UP states can also be classified into subtypes is not known. Here, we analysed neural ensemble activity from the medial prefrontal cortex from rats trained to run a spatial sequence-memory task. Application of the hidden Markov model (HMM) with three states to epochs of UP–DOWN oscillations identified DOWN states and two subtypes of UP state (UP-1 and UP-2). The two UP subtypes were distinguished by differences in duration, with UP-1 having a longer duration than UP-2, as well as differences in the speed of population vector (PV) decorrelation, with UP-1 decorrelating more slowly than UP-2. Reactivation of recent memory sequences predominantly occurred in UP-2. Short-duration reactivating UP states were dominated by UP-2 whereas long-duration ones exhibit transitions from UP-1 to UP-2. Thus, recent memory reactivation, if it occurred within long-duration UP states, typically was preceded by a period of slow PV evolution not related to recent experience, and which we speculate may be related to previously encoded information. If that is the case, then the transition from UP-1 to UP-2 subtypes may help gradual integration of recent experience with pre-existing cortical memories by interleaving the two in the same UP state. This article is part of the Theo Murphy meeting issue ‘Memory reactivation: replaying events past, present and future'.


2020 ◽  
pp. 1-34
Author(s):  
Stefan Berti ◽  
Behrang Keshavarz

Abstract Moving visual stimuli can elicit the sensation of self-motion in stationary observers, a phenomenon commonly referred to as vection. Despite the long history of vection research, the neuro-cognitive processes underlying vection have only recently gained increasing attention. Various neuropsychological techniques such as functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) have been used to investigate the temporal and spatial characteristics of the neuro-cognitive processing during vection in healthy participants. These neuropsychological studies allow for the identification of different neuro-cognitive correlates of vection, which (a) will help to unravel the neural basis of vection and (b) offer opportunities for applying vection as a tool in other research areas. The purpose of the current review is to evaluate these studies in order to show the advances in neuropsychological vection research and the challenges that lie ahead. The overview of the literature will also demonstrate the large methodological variability within this research domain, limiting the integration of results. Next, we will summarize methodological considerations and suggest helpful recommendations for future vection research, which may help to enhance the comparability across neuropsychological vection studies.


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