Primate somatosensory cortical neurons are entrained to both spontaneous and peripherally evoked spindle oscillations

Recurrent thalamocortical circuits produce a number of rhythms critical to brain function. In slow-wave sleep, spindles (7–16 Hz) are a prominent spontaneous oscillation generated by thalamic circuits and triggered by cortical slow waves. In wakefulness and under anesthesia, brief peripheral sensory stimuli can evoke 10-Hz reverberations due potentially to similar thalamic mechanisms. Functionally, sleep spindles and peripherally evoked spindles may play a role in memory consolidation and perception, respectively. Yet, rarely have the circuits involved in these two rhythms been compared in the same animals and never in primates. Here, we investigated the entrainment of primary somatosensory cortex (S1) neurons to both rhythms in ketamine-sedated macaques. First, we compared spontaneous spindles in sedation and natural sleep to validate the model. Then, we quantified entrainment with spike-field coherence and phase-locking statistics. We found that S1 neurons entrained to spontaneous sleep spindles were also entrained to the evoked spindles, although entrainment strength and phase systematically differed. Our results indicate that the spindle oscillations triggered by top-down spontaneous cortical activity and bottom-up peripheral input share a common cortical substrate. NEW & NOTEWORTHY Brief sensory stimuli evoke 10-Hz oscillations in thalamocortical neuronal activity and in perceptual thresholds. The mechanisms underlying this evoked rhythm are not well understood but are thought to be similar to those generating sleep spindles. We directly compared the entrainment of cortical neurons to both spontaneous spindles and peripherally evoked oscillations in sedated monkeys. We found that the entrainment strengths to each rhythm were positively correlated, although with differing entrainment phases, implying involvement of similar networks.

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Selection of stimulus parameters for enhancing slow wave sleep events with a Neural-field theory thalamocortical computational model

10.1101/2021.02.03.429528 ◽

2021 ◽

Author(s):

Felipe A. Torres ◽

Patricio Orio ◽

María-José Escobar

Keyword(s):

Computational Model ◽

Slow Wave ◽

Memory Consolidation ◽

Closed Loop ◽

Slow Wave Sleep ◽

Brain Activity ◽

Sensory Stimulation ◽

Sleep Spindles ◽

Slow Oscillations ◽

Closed Loop Stimulation

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.

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0086 Daytime Napping and Memory Consolidation of Novel Word Learning in Children and Adults

SLEEP ◽

10.1093/sleep/zsaa056.084 ◽

2020 ◽

Vol 43 (Supplement_1) ◽

pp. A35-A35

Author(s):

E van Rijn ◽

S A Walker ◽

V C Knowland ◽

S A Cairney ◽

A D Gouws ◽

...

Keyword(s):

White Matter ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Diffusion Tensor ◽

Brain Connectivity ◽

Nrem Sleep ◽

Sleep Spindles ◽

Adults And Children ◽

Structural Brain ◽

Novel Words

Abstract Introduction Memory for novel words benefits from sleep, particularly non-rapid eye movement (NREM) sleep and its features, such as sleep spindles and slow oscillations. This is consistent with systems consolidation models, in which sleep supports transfer from hippocampal to neocortical memory networks. Larger amounts of slow wave sleep in children has been proposed to account for enhanced consolidation effects, but such studies have typically focused on nocturnal sleep. We examined whether daytime naps benefit word retention in adults and children aged 10–12 years, and whether this relationship in children is affected by differences in white matter pathway microstructure. We hypothesized that the link between memory consolidation and structural brain connectivity will be mediated by the degree of sleep spindles during the nap. Methods Adults (N = 31; mean age = 20.91, SD = 1.55) and children (N = 38; mean age = 11.95, SD = 0.88) learned spoken novel words, followed by a 90-minute nap opportunity monitored with polysomnography. Memory for the words was tested pre- and post-nap. Children’s structural brain connectivity was measured using diffusion tensor imaging (DTI). Results Word memory was preserved following sleep in adults, while an adult wake control condition showed deterioration. Similarly, in children memory performance was stable over the nap, with wake control data currently being collected. Analyses relating behavioral changes over the nap to NREM sleep features and structural brain connectivity will be presented. Conclusion In line with sleep-dependent memory consolidation models, daytime naps protect novel words from forgetting in adults and children. Examining potential relationships between nap-based consolidation and structural integrity has important theoretical implications, given the increase in brain connectivity in language areas during childhood, as well as white matter alterations in developmental populations. Support This research was supported by the UK Economic and Social Research Council, grant no. ES/N009924/1.

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Selection of stimulus parameters for enhancing slow wave sleep events with a neural-field theory thalamocortical model

PLoS Computational Biology ◽

10.1371/journal.pcbi.1008758 ◽

2021 ◽

Vol 17 (7) ◽

pp. e1008758

Author(s):

Felipe A. Torres ◽

Patricio Orio ◽

María-José Escobar

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Closed Loop ◽

Slow Wave Sleep ◽

Brain Activity ◽

Sleep Spindles ◽

Mean Field Model ◽

Cross Point ◽

Slow Oscillations ◽

Closed Loop Stimulation

Slow-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 0°, 45°, and 90° of the phase of the narrow-band filtered ongoing activity, at 0.85 Hz as central frequency. The 0° stimulation produces better results in the power and number of SO and SP than the rhythmic or random stimulation. On the other hand, stimulating at 45° or 90° change the timing distribution of spindles centers but with fewer co-occurrences than rhythmic and 0° 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.

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Dysfunctional Overnight Memory Consolidation in Patients with Schizophrenia in Comparison to Healthy Controls: Disturbed Slow-Wave Sleep as Contributing Factor?

Neuropsychobiology ◽

10.1159/000517858 ◽

2021 ◽

pp. 1-12

Author(s):

Sara Lena Weinhold ◽

Julia Lechinger ◽

Jasper Ittel ◽

Romina Ritzenhoff ◽

Henning Johannes Drews ◽

...

Keyword(s):

Linear Relationship ◽

Slow Wave ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Declarative Memory ◽

Sleep Spindles ◽

Sleep Spindle ◽

Delta Power ◽

Sleep Parameters ◽

Spindle Power

Introduction: Memory deficiency has been shown in schizophrenia patients, but results on the role of sleep parameters in overnight consolidation of associative verbal memory are still missing. Therefore, the aim of our study was to elucidate underlying processes of impaired sleep-related consolidation of associative word pairs in schizophrenia including standard sleep parameters as well as sleep spindle counts and spectral analysis. Methods: Eighteen stably medicated schizophrenia patients and 24 healthy age-matched controls performed an associative declarative memory task before and after polysomnographic recordings. Part of the participants expected verbal associative memory testing in the morning, while the others did not. Furthermore, participants filled in self-rating questionnaires of schizophrenia-typical experiences (Eppendorf Schizophrenia Inventory [ESI] and Psychotic Symptom Rating Scale). Results: Schizophrenia patients performed worse in verbal declarative memory in the evening as well as in overnight consolidation (morning compared to evening performance). While duration of slow-wave sleep was nearly comparable between groups, schizophrenia patients showed lower sleep spindle count, reduced delta power during slow-wave sleep, and reduced spindle power during the slow oscillation (SO) up-state. In healthy but not in schizophrenia patients, a linear relationship between overnight memory consolidation and slow-wave sleep duration as well as delta power was evident. No significant effect with respect to the expectation of memory retrieval was evident in our data. Additionally, we observed a negative linear relationship between total number of sleep spindles and ESI score in healthy participants. Discussion/Conclusion: As expected, schizophrenia patients showed deficient overnight verbal declarative memory consolidation as compared to healthy controls. Reduced sleep spindles, delta power, and spindle power during the SO up-state may link sleep and memory deficiency in schizophrenia. Additionally, the absence of a linear relationship between sleep-related memory consolidation and slow-wave sleep as well as delta power suggests further functional impairments in schizophrenia. Note that this conclusion is based on observational data. Future studies should investigate if stimulation of delta waves during sleep could improve memory performance and thereby quality of life in schizophrenia.

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Effects of Olanzapine on Slow Wave Sleep, Sleep Spindles and Sleep-Related Memory Consolidation in Schizophrenia

Pharmacopsychiatry ◽

10.1055/s-2007-1004592 ◽

2008 ◽

Vol 41 (3) ◽

pp. 92-99 ◽

Cited By ~ 47

Author(s):

R. Göder ◽

G. Fritzer ◽

B. Gottwald ◽

B. Lippmann ◽

M. Seeck-Hirschner ◽

...

Keyword(s):

Slow Wave ◽

Memory Consolidation ◽

Slow Wave Sleep ◽

Sleep Spindles

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Sleep spindles facilitate selective memory consolidation

10.1101/2020.04.03.022434 ◽

2020 ◽

Cited By ~ 4

Author(s):

Dan Denis ◽

Dimitris Mylonas ◽

Craig Poskanzer ◽

Verda Bursal ◽

Jessica D. Payne ◽

...

Keyword(s):

Memory Consolidation ◽

Slow Wave Sleep ◽

Sleep Spindles ◽

Slow Oscillations ◽

Initial Strength ◽

Long Term Storage ◽

Cortical Oscillations ◽

Memory Traces ◽

New Evidence ◽

The Brain

AbstractSleep has been shown to be critical for memory consolidation, and recent research has demonstrated that this consolidation effect is selective, with certain memories being prioritized for strengthening. Initial strength of a memory appears to be one metric the brain uses to prioritize memory traces for sleep-based consolidation, but the role of consolidation-mediating cortical oscillations, such as sleep spindles and slow oscillations, has not been explored. Here, N=54 participants studied pairs of words to three distinct encoding strengths, with recall being tested immediately following learning and again six hours later. N=36 had a two-hour afternoon nap opportunity following learning, whilst the remaining (n=18) remained awake throughout. Results showed a selective benefit of sleep on memory, with sleep preferentially consolidating weakly encoded items (p=.003). The magnitude of this effect (d=0.90, 95% CI=0.29-1.50) was similar when compared to a previous study examining the benefits of a full night of sleep (d=1.36, 95% CI=0.59-2.12). Within the nap group, consolidation of weakly encoded items was associated with sleep spindle density during slow wave sleep (r=.48, p=.003). This association was present when separately examining spindles coupled (r=.41, p=.013), and uncoupled (r=.44, p=.007) with slow oscillations. Memory was significantly better in individuals who showed an amount of slow oscillation-spindle coupling that was greater than what would be expected by chance (p=.006, d=1.15). These relationships were unique to weakly encoded items, with spindles not correlating with memory for intermediate or strong items. This suggests that sleep spindles facilitate selective memory consolidation, guided in part by memory strength.Significance statementGiven the countless pieces of information we encode each day, how does the brain select which memories to commit to long-term storage? Sleep is known to aid in memory consolidation, but less research has examined which memories are prioritized to receive this benefit. Here, we found that compared to staying awake, sleep was associated with better memory for weakly encoded information. This suggests sleep helps to rescue weak memory traces from being forgotten. Sleep spindles, a hallmark oscillation of non-rapid eye movement sleep, mediates consolidation processes. We extended this to show that spindles selectively facilitated consolidation of weakly encoded memories. This provides new evidence for the selective nature of sleep-based consolidation and elucidates a physiological correlate of this preferential benefit.

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Heterogeneous origins of human sleep spindles in different cortical layers

10.1101/221234 ◽

2017 ◽

Cited By ~ 1

Author(s):

Donald J. Hagler ◽

Istvan Ulbert ◽

Lucia Wittner ◽

Lorand Erőss ◽

Joseph R. Madsen ◽

...

Keyword(s):

Memory Consolidation ◽

Slow Wave Sleep ◽

Current Source ◽

Microelectrode Arrays ◽

Phase Relationship ◽

Gamma Activity ◽

Sleep Spindles ◽

Cortical Layers ◽

Human Sleep ◽

Deep Source

AbstractSleep spindles are a cardinal feature in human slow wave sleep and may be important for memory consolidation. We studied the intracortical organization of spindles in humans by recording spontaneous sleep spindles from different cortical layers using linear microelectrode arrays. Two patterns of spindle generation were identified using visual inspection, and confirmed with factor analysis. Spindles were largest and most common in upper and middle channels, with limited involvement of deep channels. Many spindles were observed in only upper or only middle channels, but about half occurred in both. In spindles involving both middle and upper channels, the spindle envelope onset in middle channels led upper by ∼25-50ms on average. The phase relationship between spindle waves in upper and middle channels varied dynamically within spindle epochs, and across individuals. Current source density analysis demonstrated that upper and middle channel spindles were both generated by an excitatory supragranular current sink while an additional deep source was present for middle channel spindles only. Only middle channel spindles were accompanied by deep gamma activity. These results suggest that upper channel spindles are generated by supragranular pyramids, and middle channel by infragranular. Possibly, middle channel spindles are generated by core thalamocortical afferents, and upper channel by matrix. The concurrence of these patterns could reflect engagement of cortical circuits in the integration of more focal (core) and distributed (matrix) aspects of memory. These results demonstrate that at least two distinct intracortical systems generate human sleep spindles.Significance StatementBursts of ∼14Hz oscillations, lasting about a second, have been recognized for over 80 years as cardinal features of mammalian sleep. Recent findings suggest that they play a key role in organizing cortical activity during memory consolidation. We used linear microelectrode arrays to study their intracortical organization in humans. We found that spindles could be divided into two types. One mainly engages upper layers of the cortex, which are considered to be specialized for associative activity. The other engages both upper and middle layers, including those devoted to sensory input. The interaction of these two spindle types may help organize the interaction of sensory and associative aspects of memory consolidation.

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Intra- and interregional cortical interactions related to sharp-wave ripples and dentate spikes

Journal of Neurophysiology ◽

10.1152/jn.00644.2016 ◽

2017 ◽

Vol 117 (2) ◽

pp. 556-565 ◽

Cited By ~ 15

Author(s):

Drew B. Headley ◽

Vasiliki Kanta ◽

Denis Paré

Keyword(s):

Memory Consolidation ◽

Cortical Neurons ◽

Slow Wave Sleep ◽

Dorsal Hippocampus ◽

Gamma Oscillations ◽

Sharp Wave ◽

Up States ◽

Gamma Coherence ◽

Cortical Regions ◽

The Relationship

The hippocampus generates population events termed sharp-wave ripples (SWRs) and dentate spikes (DSs). While little is known about DSs, SWR-related hippocampal discharges during sleep are thought to replay prior waking activity, reactivating the cortical networks that encoded the initial experience. During slow-wave sleep, such reactivations likely occur during up-states, when most cortical neurons are depolarized. However, most studies have examined the relationship between SWRs and up-states measured in single neocortical regions. As a result, it is currently unclear whether SWRs are associated with particular patterns of widely distributed cortical activity. Additionally, no such investigation has been carried out for DSs. The present study addressed these questions by recording SWRs and DSs from the dorsal hippocampus simultaneously with prefrontal, sensory (visual and auditory), perirhinal, and entorhinal cortices in naturally sleeping rats. We found that SWRs and DSs were associated with up-states in all cortical regions. Up-states coinciding with DSs and SWRs exhibited increased unit activity, power in the gamma band, and intraregional gamma coherence. Unexpectedly, interregional gamma coherence rose much more strongly in relation to DSs than to SWRs. Whereas the increase in gamma coherence was time locked to DSs, that seen in relation to SWRs was not. These observations suggest that SWRs are related to the strength of up-state activation within individual regions throughout the neocortex but not so much to gamma coherence between different regions. Perhaps more importantly, DSs coincided with stronger periods of interregional gamma coherence, suggesting that they play a more important role than previously assumed. NEW & NOTEWORTHY Off-line cortico-hippocampal interactions are thought to support memory consolidation. We surveyed the relationship between hippocampal sharp-wave ripples (SWRs) and dentate spikes (DSs) with up-states across multiple cortical regions. SWRs and DSs were associated with increased cortical gamma oscillations. Interregional gamma coherence rose much more strongly in relation to DSs than to SWRs. Moreover, it was time locked to DSs but not SWRs. These results have important implications for current theories of systems memory consolidation during sleep.

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