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

2017 ◽  
Vol 117 (2) ◽  
pp. 556-565 ◽  
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.

scholarly journals Bidirectional Interaction of Hippocampal Ripples and Cortical Slow Waves Leads to Coordinated Spiking Activity During NREM Sleep

2020 ◽  
Vol 31 (1) ◽  
pp. 324-340
Author(s):  
Pavel Sanda ◽  
Paola Malerba ◽  
Xi Jiang ◽  
Giri P Krishnan ◽  
Jorge Gonzalez-Martinez ◽  
...  
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Nrem Sleep ◽  
Slow Waves ◽  
Slow Oscillation ◽  
Cortical Input ◽  
Sharp Wave ◽  
Up States ◽  
Intracranial Recordings

Abstract The dialogue between cortex and hippocampus is known to be crucial for sleep-dependent memory consolidation. During slow wave sleep, memory replay depends on slow oscillation (SO) and spindles in the (neo)cortex and sharp wave-ripples (SWRs) in the hippocampus. The mechanisms underlying interaction of these rhythms are poorly understood. We examined the interaction between cortical SO and hippocampal SWRs in a model of the hippocampo–cortico–thalamic network and compared the results with human intracranial recordings during sleep. We observed that ripple occurrence peaked following the onset of an Up-state of SO and that cortical input to hippocampus was crucial to maintain this relationship. A small fraction of ripples occurred during the Down-state and controlled initiation of the next Up-state. We observed that the effect of ripple depends on its precise timing, which supports the idea that ripples occurring at different phases of SO might serve different functions, particularly in the context of encoding the new and reactivation of the old memories during memory consolidation. The study revealed complex bidirectional interaction of SWRs and SO in which early hippocampal ripples influence transitions to Up-state, while cortical Up-states control occurrence of the later ripples, which in turn influence transition to Down-state.

scholarly journals 0084 Sleep Consolidates Incidentally Encoded Information After Deep but Not Shallow Encoding

SLEEP ◽  
2020 ◽  
Vol 43 (Supplement_1) ◽  
pp. A34-A34
Author(s):  
E M Wernette ◽  
K M Fenn
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Declarative Memory ◽  
Memory Performance ◽  
Memory Test ◽  
Memory Traces ◽  
Incidental Encoding ◽  
The Relationship ◽  
With Memory

Abstract Introduction Slow wave sleep (SWS) strengthens declarative memory for information studied for a later test. However, research on the effect of sleep on information that is not intentionally remembered is scare. Previous research from our lab suggests sleep consolidates some, but not all, information that has been encoded incidentally, meaning that it has been acted on but not intentionally remembered. It remains unclear what determines which information benefits from sleep-dependent consolidation processes and what aspects of sleep are related to these mnemonic benefits. In two experiments, we test the hypothesis that sleep consolidates strong but not weak memory traces following incidental encoding, and assess the relationship between memory performance and objective sleep characteristics. Methods In Experiment 1, participants rated words one (weak traces) or three times (strong traces) in a deep or shallow incidental encoding task. Participants either rated words on a scale from ‘concrete’ to ‘abstract’ (deep) or counted the vowels in the words (shallow). Following a 12-hour period containing sleep or wakefulness, participants took a surprise memory test. In Experiment 2, participants rated words one or three times in the deep encoding task, received an 8-hour sleep opportunity with polysomnography, and took the surprise memory test. Results In Experiment 1, participants remembered words better after sleep than wake regardless of whether words were encoded one or three times, but only after deep encoding. Sleep did not consolidate information following shallow encoding. Experiment 2 is ongoing, but we predict that the amount of SWS will correlate positively with memory. Conclusion Results thus far suggest sleep may have consolidated information based on the strength of memory traces. Because deep encoding results in stronger memory traces than shallow encoding, this work is broadly consistent with theories of memory consolidation that predict sleep is more beneficial for strong memory traces than weak, such as the synaptic downscaling hypothesis. Support N/A

scholarly journals Replay of large-scale spatio-temporal patterns from waking during subsequent slow-wave sleep in human cortex

2017 ◽  
Author(s):  
Xi Jiang ◽  
Isaac Shamie ◽  
Werner Doyle ◽  
Daniel Friedman ◽  
Patricia Dugan ◽  
...  
Keyword(s):  
Slow Wave ◽  
Memory Consolidation ◽  
Animal Studies ◽  
Large Scale ◽  
Slow Wave Sleep ◽  
Cognitive Task ◽  
Human Memory ◽  
Sharp Wave ◽  
Direct Demonstration ◽  
Spatio Temporal

AbstractAnimal studies support the hypothesis that in slow-wave sleep, replay of waking neocortical activity under hippocampal guidance leads to memory consolidation. However, no intracranial electrophysiological evidence for replay exists in humans. We identified consistent sequences of population firing peaks across widespread cortical regions during complete waking periods. The occurrence of these Motifs were compared between sleeps preceding the waking period (Sleep-Pre) when the Motifs were identified, and those following (Sleep-Post). In all subjects, the majority of waking Motifs (most of which were novel) had more matches in Sleep-Post than in Sleep-Pre. In rodents, hippocampal replay occurs during local sharp-wave ripples, and the associated neocortical replay tends to occur during local sleep spindles and down-to-up transitions. These waves may facilitate consolidation by sequencing cell-firing and encouraging plasticity. Similarly, we found that Motifs were coupled to neocortical spindles, down-to-up transitions, theta bursts, and hippocampal sharp-wave ripples. While Motifs occurring during cognitive task performance were more likely to have more matches in subsequent sleep, our studies provide no direct demonstration that the replay of Motifs contributes to consolidation. Nonetheless, these results confirm a core prediction of the dominant neurobiological theory of human memory consolidation.

scholarly journals LFP clustering in cortex reveals a taxonomy of Up states and near-millisecond, ordered phase-locking in cortical neurons

2019 ◽  
Vol 122 (4) ◽  
pp. 1794-1809
Author(s):  
Catalin C. Mitelut ◽  
Martin A. Spacek ◽  
Allen W. Chan ◽  
Tim H. Murphy ◽  
Nicholas V. Swindale
Keyword(s):  
Local Field ◽  
Local Field Potential ◽  
Cortical Neurons ◽  
State Transition ◽  
Slow Wave Sleep ◽  
Field Potential ◽  
State Transitions ◽  
Wide Field ◽  
Cortical Function ◽  
Up States

During slow-wave sleep and anesthesia, mammalian cortex exhibits a synchronized state during which neurons shift from a largely nonfiring to a firing state, known as an Up-state transition. Up-state transitions may constitute the default activity pattern of the entire cortex (Neske GT. Front Neural Circuits 9: 88, 2016) and could be critical to understanding cortical function, yet the genesis of such transitions and their interaction with single neurons is not well understood. It was recently shown that neurons firing at rates >2 Hz fire spikes in a stereotyped order during Up-state transitions (Luczak A, McNaughton BL, Harris KD. Nat Rev Neurosci 16: 745–755, 2015), yet it is still unknown if Up states are homogeneous and whether spiking order is present in neurons with rates <2 Hz (the majority). Using extracellular recordings from anesthetized cats and mice and from naturally sleeping rats, we show for the first time that Up-state transitions can be classified into several types based on the shape of the local field potential (LFP) during each transition. Individual LFP events could be localized in time to within 1–4 ms, more than an order of magnitude less than in previous studies. The majority of recorded neurons synchronized their firing to within ±5–15 ms relative to each Up-state transition. Simultaneous electrophysiology and wide-field imaging in mouse confirmed that LFP event clusters are cortex-wide phenomena. Our findings show that Up states are of different types and point to the potential importance of temporal order and millisecond-scale signaling by cortical neurons. NEW & NOTEWORTHY During cortical Up-state transitions in sleep and anesthesia, neurons undergo brief periods of increased firing in an order similar to that occurring in awake states. We show that these transitions can be classified into distinct types based on the shape of the local field potential. Transition times can be defined to <5 ms. Most neurons synchronize their firing to within ±5–15 ms of the transitions and fire in a consistent order.

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

2020 ◽  
Vol 123 (1) ◽  
pp. 300-307 ◽  
Author(s):  
Srihari Y. Sritharan ◽  
Enrique Contreras-Hernández ◽  
Andrew G. Richardson ◽  
Timothy H. Lucas
Keyword(s):  
Memory Consolidation ◽  
Cortical Neurons ◽  
Brain Function ◽  
Slow Wave Sleep ◽  
Phase Locking ◽  
Sleep Spindles ◽  
Sensory Stimuli ◽  
Spontaneous Oscillation ◽  
Peripheral Sensory ◽  
Field Coherence

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.

032 Sleep Consolidates Memory for Strong but not Weak Information After Incidental Encoding

SLEEP ◽  
2021 ◽  
Vol 44 (Supplement_2) ◽  
pp. A14-A15
Author(s):  
Elle Wernette ◽  
Kimberly Fenn
Keyword(s):  
Slow Wave ◽  
Response Latency ◽  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Memory Performance ◽  
Memory Test ◽  
Memory Strength ◽  
Memory Traces ◽  
Incidental Encoding ◽  
The Relationship

Abstract Introduction Slow wave sleep (SWS) strengthens memory for studied information, but research on the effect of sleep on information that is not intentionally remembered is scarce. Previous research from our lab suggests sleep consolidates some information that has been encoded incidentally, meaning that it has been acted on but not intentionally remembered. It remains unclear what determines which information is consolidated during sleep after incidental encoding and what aspects of sleep are related to this mnemonic benefit. In two experiments, we test the hypothesis that sleep consolidates strong but not weak memory traces following incidental encoding and assess the relationship between memory performance and sleep attributes. Methods In Experiment 1, we manipulated memory strength within- and between-subjects. Participants rated words one or three times (within) in a shallow or deep incidental encoding task (between). In the shallow task, participants counted vowels in each word; in the deep task, participants rated each word on a scale from ‘concrete’ to ‘abstract’. Following a 12-hour period containing sleep or wakefulness, participants took a surprise memory test. In Experiment 2, participants rated words one or three times in the deep encoding task, received an 8-hour sleep opportunity with partial PSG, and took the surprise memory test. Results In Experiment 1, participants remembered words better after sleep than wake regardless of number of encoding trials, but only after deep encoding. There was not an effect of sleep following shallow encoding. In Experiment 2, SWS correlated negatively with response latency for correctly recognized words encoded once, but not those encoded three times. That is, participants who received more SWS showed faster performance. Conclusion Results suggest sleep consolidated information based on the depth of encoding, and this benefit was related to SWS. This work is broadly consistent with theories of memory consolidation that predict sleep is more beneficial for strong than weak memory traces, such as the synaptic downscaling hypothesis. Support (if any):

scholarly journals Sharp wave-associated activity patterns of olfactory cortical neurons in the mouse piriform cortex

2018 ◽  
Author(s):  
Kazuki Katori ◽  
Hiroyuki Manabe ◽  
Ai Nakashima ◽  
Eer Dunfu ◽  
Takuya Sasaki ◽  
...  
Keyword(s):  
Cortical Neurons ◽  
Slow Wave Sleep ◽  
Activity Patterns ◽  
Piriform Cortex ◽  
Associative Memories ◽  
Firing Rates ◽  
Anterior Piriform Cortex ◽  
Sharp Wave ◽  
Sharp Waves ◽  
Neural Activities

ABSTRACTThe olfactory piriform cortex is thought to participate in olfactory associative memory. Like the hippocampus, which is essential for episodic memory, it belongs to an evolutionally conserved paleocortex and comprises a three-layered cortical structure. During slow-wave sleep, the olfactory piriform cortex becomes less responsive to external odor stimuli and instead displays sharp wave (SPW) activity similar to that observed in the hippocampus. Neural activity patterns during hippocampal SPW have been intensively studied in terms of memory consolidation; however, little is known about the activity patterns of olfactory cortical neurons during olfactory cortex sharp waves (OC-SPWs). In this study, we recorded multi-unit neural activities in the anterior piriform cortex in urethane-anesthetized mice. We found that the activity patterns of olfactory cortical neurons during OC-SPWs were non-randomly organized. Individual olfactory cortical neurons varied in the timings of their peak firing rates during OC-SPW events. Moreover, specific pairs of olfactory cortical neurons were more frequently activated together than expected by chance. On the basis of these observations, we speculate that coordinated activation of specific subsets of olfactory cortical neurons repeats during OC-SPWs, thereby facilitating synaptic plasticity underlying the consolidation of olfactory associative memories.

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