scholarly journals Nested sequences of hippocampal assemblies during behavior support subsequent sleep replay

Science ◽  
2018 ◽  
Vol 362 (6415) ◽  
pp. 675-679 ◽  
Author(s):  
Céline Drieu ◽  
Ralitsa Todorova ◽  
Michaël Zugaro

Consolidation of spatial and episodic memories is thought to rely on replay of neuronal activity sequences during sleep. However, the network dynamics underlying the initial storage of memories during wakefulness have never been tested. Although slow, behavioral time scale sequences have been claimed to sustain sequential memory formation, fast (“theta”) time scale sequences, nested within slow sequences, could be instrumental. We found that in rats traveling passively on a model train, place cells formed behavioral time scale sequences but theta sequences were degraded, resulting in impaired subsequent sleep replay. In contrast, when the rats actively ran on a treadmill while being transported on the train, place cells generated clear theta sequences and accurate trajectory replay during sleep. Our results support the view that nested sequences underlie the initial formation of memory traces subsequently consolidated during sleep.

2021 ◽  
Author(s):  
Luendreo Barboza ◽  
Benjamin Bessieres ◽  
Omina Nazarzoda ◽  
Cristina Alberini

The formation of long-term episodic memories requires the activation of molecular mechanisms in several regions of the medial temporal lobe, including the hippocampus and anterior cingulate cortex (ACC). The extent to which these regions engage distinct mechanisms and cell types to support memory formation is not well understood. Recent studies reported that oligodendrogenesis is essential for learning and long-term memory; however, whether these mechanisms are required only in selected brain regions is still unclear. Also still unknown are the temporal kinetics of engagement of learning-induced oligodendrogenesis and whether this oligodendrogenesis occurs in response to neuronal activity. Here we show that in rats and mice, episodic learning rapidly increases the oligodendrogenesis and myelin biogenesis transcripts olig2, myrf, mbp, and plp1, as well as oligodendrogenesis, in the ACC but not in the dorsal hippocampus (dHC). Region-specific knockdown and knockout of Myrf, a master regulator of oligodendrocyte maturation, revealed that oligodendrogenesis is required for memory formation in the ACC but not the dHC. Chemogenetic neuronal silencing in the ACC showed that neuronal activity is critical for learning-induced oligodendrogenesis. Hence, an activity-dependent increase in oligodendrogenesis in selected brain regions, specifically in the ACC but not dHC, is critical for the formation of episodic memories.


2015 ◽  
Vol 18 (12) ◽  
pp. 1780-1788 ◽  
Author(s):  
Kenta M Hagihara ◽  
Tomonari Murakami ◽  
Takashi Yoshida ◽  
Yoshiaki Tagawa ◽  
Kenichi Ohki

2020 ◽  
Vol 118 (1) ◽  
pp. e2020810118
Author(s):  
Ye Wang ◽  
Wing-Yu Fu ◽  
Kit Cheung ◽  
Kwok-Wang Hung ◽  
Congping Chen ◽  
...  

Hippocampal synaptic plasticity is important for learning and memory formation. Homeostatic synaptic plasticity is a specific form of synaptic plasticity that is induced upon prolonged changes in neuronal activity to maintain network homeostasis. While astrocytes are important regulators of synaptic transmission and plasticity, it is largely unclear how they interact with neurons to regulate synaptic plasticity at the circuit level. Here, we show that neuronal activity blockade selectively increases the expression and secretion of IL-33 (interleukin-33) by astrocytes in the hippocampal cornu ammonis 1 (CA1) subregion. This IL-33 stimulates an increase in excitatory synapses and neurotransmission through the activation of neuronal IL-33 receptor complex and synaptic recruitment of the scaffold protein PSD-95. We found that acute administration of tetrodotoxin in hippocampal slices or inhibition of hippocampal CA1 excitatory neurons by optogenetic manipulation increases IL-33 expression in CA1 astrocytes. Furthermore, IL-33 administration in vivo promotes the formation of functional excitatory synapses in hippocampal CA1 neurons, whereas conditional knockout of IL-33 in CA1 astrocytes decreases the number of excitatory synapses therein. Importantly, blockade of IL-33 and its receptor signaling in vivo by intracerebroventricular administration of its decoy receptor inhibits homeostatic synaptic plasticity in CA1 pyramidal neurons and impairs spatial memory formation in mice. These results collectively reveal an important role of astrocytic IL-33 in mediating the negative-feedback signaling mechanism in homeostatic synaptic plasticity, providing insights into how astrocytes maintain hippocampal network homeostasis.


2017 ◽  
Vol 8 (1) ◽  
Author(s):  
Nicolette Ognjanovski ◽  
Samantha Schaeffer ◽  
Jiaxing Wu ◽  
Sima Mofakham ◽  
Daniel Maruyama ◽  
...  

Abstract Activity in hippocampal area CA1 is essential for consolidating episodic memories, but it is unclear how CA1 activity patterns drive memory formation. We find that in the hours following single-trial contextual fear conditioning (CFC), fast-spiking interneurons (which typically express parvalbumin (PV)) show greater firing coherence with CA1 network oscillations. Post-CFC inhibition of PV+ interneurons blocks fear memory consolidation. This effect is associated with loss of two network changes associated with normal consolidation: (1) augmented sleep-associated delta (0.5–4 Hz), theta (4–12 Hz) and ripple (150–250 Hz) oscillations; and (2) stabilization of CA1 neurons’ functional connectivity patterns. Rhythmic activation of PV+ interneurons increases CA1 network coherence and leads to a sustained increase in the strength and stability of functional connections between neurons. Our results suggest that immediately following learning, PV+ interneurons drive CA1 oscillations and reactivation of CA1 ensembles, which directly promotes network plasticity and long-term memory formation.


2013 ◽  
Vol 36 (6) ◽  
pp. 610-611 ◽  
Author(s):  
Sen Cheng ◽  
Markus Werning

AbstractWe propose that rapid eye movement (REM) and slow-wave sleep contribute differently to the formation of episodic memories. REM sleep is important for building up invariant object representations that eventually recur to gamma-band oscillations in the neocortex. In contrast, slow-wave sleep is more directly involved in the consolidation of episodic memories through replay of sequential neural activity in hippocampal place cells.


2020 ◽  
Author(s):  
Fahd Yazin ◽  
Moumita Das ◽  
Arpan Banerjee ◽  
Dipanjan Roy

AbstractEpisodic memories are contextual experiences ordered in time. This is underpinned by associative binding between events within the same contexts. The role of prediction errors in strengthening declarative memory is well established but has not been investigated in the time dimension of complex episodic memories. Here we used 3-day movie viewing paradigm to test the hypothesis that contextual prediction errors leads to temporal organization of sequential memory processing. Our main findings uncover that prediction errors lead to changes in temporal organization of events, secondly, new unexpected sequences show as high accuracy as control sequences viewed repeatedly, and these effects are specifically due to prediction errors, and not novel associations. A drift-diffusion modelling further revealed a lower decision threshold for the newer, unexpected sequences compared to older sequences reflected by their faster recall leads to reorganization of episodes in time. Moreover, we found individual decision threshold could significantly predict their relative speed of sequence memory recall. Taking together our results suggest a temporally distinct role for prediction errors in ordering sequences of events in episodic memory.


2020 ◽  
Author(s):  
Yvonne Y. Chen ◽  
Daniel Yoshor ◽  
Sameer A. Sheth ◽  
Brett L. Foster

AbstractPeriods of cognitive disengagement, such as rest or sleep, are thought to support the progressive consolidation of episodic memories. During these states, the hippocampus displays transient high-frequency oscillatory bursts, known as ripples, which are thought to promote interactions with the neocortex, consolidating memory traces. More recent findings have suggested ripples in the human hippocampus may also occur during task engagement, particularly for tasks requiring episodic memory processes. However, it is unclear if hippocampal ripples occur during other cognitive states or whether ripple properties are modulated by specific types of task demands. In addition, identifying genuine hippocampal ripple events in the human brain can be methodological challenging. To address these questions, we used intracranial recordings from the human hippocampus to quantify ripple events across perceptual, memory and resting task states. Using spectro-temporal identification of hippocampal ripples, we observed highly similar ripple event properties across tasks, with a modest yet significant increase in ripple properties (rate, duration & amplitude) during resting task states. These ripple event attributes did not differ between hemisphere, nor across or within the time of day examined. Supporting data further highlighted that while hippocampal ripples occurred during all task states, these rates were typically lower than that observed during sleep. Together, these findings highlight that hippocampal ripples occur consistently, but sparsely, during a broad range of cognitive task states. Such findings may be incorporated into existing models of systems consolidation, whereby hippocampal ripples help to initially establish latent memory traces.


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