scholarly journals Network resonance during slow-wave sleep facilitates memory consolidation through phase-coding

2019 ◽  
Author(s):  
Quinton M. Skilling ◽  
Brittany C. Clawson ◽  
Bolaji Eniwaye ◽  
James Shaver ◽  
Nicolette Ognjanovski ◽  
...  
Keyword(s):  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Critical Role ◽  
Spike Timing ◽  
Network Activity ◽  
Theta Band ◽  
Phase Coding ◽  
Neuronal Populations ◽  
Network Oscillations ◽  
Memory Representations

AbstractSleep plays a critical role in memory consolidation, however, the exact role that sleep and its effects on neural network dynamics play in this process is still unclear. Here, we combine computational and experimental approaches to study the dynamical, network-wide underpinnings of hippocampal memory consolidation during sleep. We provide data to support a novel hypothesis on the role of cellular resonance with sleep-associated theta band (4-12 Hz) hippocampal oscillations in this process. We show that increases in the stability of hippocampal memory representations after learning (which predicts successful memory consolidation) are mediated through emergent network-wide resonance and locking of neuronal activity to network oscillations. These changes arise in the network as a function of changes to network structure during learning, and mirror experimental findings in the hippocampus. Finally, we show that input-dependent pattern formation (e.g. “replay”) in the hippocampus during sleep states, together with spike timing dependent plasticity (STDP)-based memory consolidation, leads to universal network activity reorganization. This reorganization generates heterogeneous changes in neuronal spiking frequency, similar to what has been observed in a variety of brain circuits across periods of sleep. Our results support the hypothesis that sleep plays an active role in memory consolidation by switching the hippocampal network from rate-based to phase-based information representation. The mechanisms through which this occurs supports the integration of heterogeneous cell populations into memory traces.Significance StatementIn this study, we provide a mechanistic explanation of how sleep selectively facilitates memory consolidation, through recruitment of heterogeneous neuronal populations and structural reorganization of the network into an engram. Specifically, we show that emergent theta band oscillations during sleep facilitate stabilization of memory representations via spike timing dependent reinforcement. This stabilization, together with STDP, allows for systematic reorganization of synaptic connections within these populations, universally redistributing firing rates of participating neurons. Simultaneously, network oscillations facilitate a switch from rate-to phase-coding of information among neuronal populations with highly heterogenous firing frequencies, incorporating more neurons into the engram. Our results reconcile discrepant findings on network reorganization during sleep, and demonstrate a clear mechanism for both strengthening and weakening of synaptic efficacy during sleep.

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

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.

Spike Timing of Lacunosom-Moleculare Targeting Interneurons and CA3 Pyramidal Cells During High-Frequency Network Oscillations In Vitro

2007 ◽  
Vol 98 (1) ◽  
pp. 96-104 ◽  
Author(s):  
Jay Spampanato ◽  
Istvan Mody
Keyword(s):  
High Frequency ◽  
Epileptiform Activity ◽  
Field Potential ◽  
Pyramidal Cells ◽  
Gamma Oscillations ◽  
Spike Timing ◽  
Network Activity ◽  
Network Oscillations ◽  
Ca3 Pyramidal Cells

Network activity in the 200- to 600-Hz range termed high-frequency oscillations (HFOs) has been detected in epileptic tissue from both humans and rodents and may underlie the mechanism of epileptogenesis in experimental rodent models. Slower network oscillations including theta and gamma oscillations as well as ripples are generated by the complex spike timing and interactions between interneurons and pyramidal cells of the hippocampus. We determined the activity of CA3 pyramidal cells, stratum oriens lacunosum-moleculare (O-LM) and s. radiatum lacunosum-moleculare (R-LM) interneurons during HFO in the in vitro low-Mg2+ model of epileptiform activity in GIN mice. In these animals, interneurons can be identified prior to cell-attached recordings by the expression of green-fluorescent protein (GFP). Simultaneous local field potential recordings from s. pyramidale and on-cell recordings of individual interneurons and principal cells revealed three primary firing behaviors of the active cells: 36% of O-LM interneurons and 60% of pyramidal cells fired action potentials at high frequencies during the HFO. R-LM interneurons were biphasic in that they fired at high frequency at the beginning of the HFO but stopped firing before its end. When considering only the highest frequency component of the oscillations most pyramidal cells fired on the rising phase of the oscillation. These data provide evidence for functional distinction during HFOs within otherwise homogeneous groups of O-LM interneurons and pyramidal cells.

scholarly journals Temporally Targeted Interactions With Pathologic Oscillations as Therapeutical Targets in Epilepsy and Beyond

2021 ◽  
Vol 15 ◽  
Author(s):  
Tamás Földi ◽  
Magor L. Lőrincz ◽  
Antal Berényi
Keyword(s):  
Neuronal Network ◽  
Epileptic Seizures ◽  
Theoretical Background ◽  
Pharmacological Therapy ◽  
Spike Timing ◽  
Network Activity ◽  
Stable States ◽  
Neuronal Network Activity ◽  
Network Oscillations ◽  
The Brain

Self-organized neuronal oscillations rely on precisely orchestrated ensemble activity in reverberating neuronal networks. Chronic, non-malignant disorders of the brain are often coupled to pathological neuronal activity patterns. In addition to the characteristic behavioral symptoms, these disturbances are giving rise to both transient and persistent changes of various brain rhythms. Increasing evidence support the causal role of these “oscillopathies” in the phenotypic emergence of the disease symptoms, identifying neuronal network oscillations as potential therapeutic targets. While the kinetics of pharmacological therapy is not suitable to compensate the disease related fine-scale disturbances of network oscillations, external biophysical modalities (e.g., electrical stimulation) can alter spike timing in a temporally precise manner. These perturbations can warp rhythmic oscillatory patterns via resonance or entrainment. Properly timed phasic stimuli can even switch between the stable states of networks acting as multistable oscillators, substantially changing the emergent oscillatory patterns. Novel transcranial electric stimulation (TES) approaches offer more reliable neuronal control by allowing higher intensities with tolerable side-effect profiles. This precise temporal steerability combined with the non- or minimally invasive nature of these novel TES interventions make them promising therapeutic candidates for functional disorders of the brain. Here we review the key experimental findings and theoretical background concerning various pathological aspects of neuronal network activity leading to the generation of epileptic seizures. The conceptual and practical state of the art of temporally targeted brain stimulation is discussed focusing on the prevention and early termination of epileptic seizures.

scholarly journals Membrane Resonance in Pyramidal and GABAergic Neurons of the Mouse Perirhinal Cortex

2021 ◽  
Vol 15 ◽  
Author(s):  
Noemi Binini ◽  
Francesca Talpo ◽  
Paolo Spaiardi ◽  
Claudia Maniezzi ◽  
Matteo Pedrazzoli ◽  
...  
Keyword(s):  
Pyramidal Neurons ◽  
Slow Wave Sleep ◽  
Perirhinal Cortex ◽  
Spike Timing ◽  
Neuronal Firing ◽  
Network Activity ◽  
Resting Potential ◽  
Memory Representation ◽  
Subthreshold Oscillations ◽  
Membrane Resonance

The perirhinal cortex (PRC) is a polymodal associative region of the temporal lobe that works as a gateway between cortical areas and hippocampus. In recent years, an increasing interest arose in the role played by the PRC in learning and memory processes, such as object recognition memory, in contrast with certain forms of hippocampus-dependent spatial and episodic memory. The integrative properties of the PRC should provide all necessary resources to select and enhance the information to be propagated to and from the hippocampus. Among these properties, we explore in this paper the ability of the PRC neurons to amplify the output voltage to current input at selected frequencies, known as membrane resonance. Within cerebral circuits the resonance of a neuron operates as a filter toward inputs signals at certain frequencies to coordinate network activity in the brain by affecting the rate of neuronal firing and the precision of spike timing. Furthermore, the ability of the PRC neurons to resonate could have a fundamental role in generating subthreshold oscillations and in the selection of cortical inputs directed to the hippocampus. Here, performing whole-cell patch-clamp recordings from perirhinal pyramidal neurons and GABAergic interneurons of GAD67-GFP+ mice, we found, for the first time, that the majority of PRC neurons are resonant at their resting potential, with a resonance frequency of 0.5–1.5 Hz at 23°C and of 1.5–2.8 Hz at 36°C. In the presence of ZD7288 (blocker of HCN channels) resonance was abolished in both pyramidal neurons and interneurons, suggesting that Ih current is critically involved in resonance generation. Otherwise, application of TTx (voltage-dependent Na+ channel blocker) attenuates the resonance in pyramidal neurons but not in interneurons, suggesting that only in pyramidal neurons the persistent sodium current has an amplifying effect. These experimental results have also been confirmed by a computational model. From a functional point of view, the resonance in the PRC would affect the reverberating activity between neocortex and hippocampus, especially during slow wave sleep, and could be involved in the redistribution and strengthening of memory representation in cortical regions.

scholarly journals Hippocampal CA2 ripples recruit social replay and promote social memory

2020 ◽  
Author(s):  
Oliva Azahara ◽  
Fernández-Ruiz Antonio ◽  
Leroy Felix ◽  
Siegelbaum A. Steven
Keyword(s):  
Spatial Memory ◽  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Social Memory ◽  
Declarative Memory ◽  
Critical Role ◽  
Sensory Information ◽  
General Mechanism ◽  
Recent Experience ◽  
Wide Range

The consolidation of spatial memory depends on the reactivation (‘replay’) of hippocampal place cells that were active during recent behavior. These reactivations are observed during sharp wave-ripples (SWRs), synchronous oscillatory events that occur during slow-wave sleep1–9 and whose disruption impairs spatial memory consolidation 4,6,7,9. Although the hippocampus encodes a wide range of non-spatial forms of declarative memory, it is not yet known whether SWRs are necessary for non-spatial memory. Moreover, although SWRs can arise from either the hippocampal CA38 or CA210 regions, the relative importance of these sources for memory consolidation is unknown. Here we examined the role of SWRs during the consolidation of social memory, the ability of an animal to recognize and remember a conspecific, focusing on CA2 because of its critical role in social memory11,12,13. We found that ensembles of CA2 pyramidal neurons that were active during social exploration of novel conspecifics were reactivated during SWRs. Importantly, disruption or enhancement of CA2 SWRs suppressed or prolonged social memory, respectively. Thus, SWR reactivation of hippocampal firing related to recent experience appears to be a general mechanism for binding spatial, temporal and sensory information into high-order memory representations.

scholarly journals About Sleep's Role in Memory

2013 ◽  
Vol 93 (2) ◽  
pp. 681-766 ◽  
Author(s):  
Björn Rasch ◽  
Jan Born
Keyword(s):  
Rem Sleep ◽  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Active Role ◽  
Brain State ◽  
Long Term Memory ◽  
Term Memory ◽  
Memory Representations ◽  
Genetic Mechanisms

Over more than a century of research has established the fact that sleep benefits the retention of memory. In this review we aim to comprehensively cover the field of “sleep and memory” research by providing a historical perspective on concepts and a discussion of more recent key findings. Whereas initial theories posed a passive role for sleep enhancing memories by protecting them from interfering stimuli, current theories highlight an active role for sleep in which memories undergo a process of system consolidation during sleep. Whereas older research concentrated on the role of rapid-eye-movement (REM) sleep, recent work has revealed the importance of slow-wave sleep (SWS) for memory consolidation and also enlightened some of the underlying electrophysiological, neurochemical, and genetic mechanisms, as well as developmental aspects in these processes. Specifically, newer findings characterize sleep as a brain state optimizing memory consolidation, in opposition to the waking brain being optimized for encoding of memories. Consolidation originates from reactivation of recently encoded neuronal memory representations, which occur during SWS and transform respective representations for integration into long-term memory. Ensuing REM sleep may stabilize transformed memories. While elaborated with respect to hippocampus-dependent memories, the concept of an active redistribution of memory representations from networks serving as temporary store into long-term stores might hold also for non-hippocampus-dependent memory, and even for nonneuronal, i.e., immunological memories, giving rise to the idea that the offline consolidation of memory during sleep represents a principle of long-term memory formation established in quite different physiological systems.

scholarly journals Sounding It Out: Auditory Stimulation and Overnight Memory Processing

2021 ◽  
Author(s):  
Marcus O. Harrington ◽  
Scott A. Cairney
Keyword(s):  
Rem Sleep ◽  
Memory Consolidation ◽  
Slow Wave Sleep ◽  
Auditory Stimulation ◽  
Theta Oscillations ◽  
Neural Oscillations ◽  
Healthy Children ◽  
Factors Affecting ◽  
Memory Processing ◽  
Eeg Recordings

Abstract Purpose of Review Auditory stimulation is a technique that can enhance neural oscillations linked to overnight memory consolidation. In this review, we evaluate the impacts of auditory stimulation on the neural oscillations of sleep and associated memory processes in a variety of populations. Recent Findings Cortical EEG recordings of slow-wave sleep (SWS) are characterised by two cardinal oscillations: slow oscillations (SOs) and sleep spindles. Auditory stimulation delivered in SWS enhances SOs and phase-coupled spindle activity in healthy children and adults, children with ADHD, adults with mild cognitive impairment and patients with major depression. Under certain conditions, auditory stimulation bolsters the benefits of SWS for memory consolidation, although further work is required to fully understand the factors affecting stimulation-related memory gains. Recent work has turned to rapid eye movement (REM) sleep, demonstrating that auditory stimulation can be used to manipulate REM sleep theta oscillations. Summary Auditory stimulation enhances oscillations linked to overnight memory processing and shows promise as a technique for enhancing the memory benefits of sleep.

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