[The role of sleep brain oscillations and neuronal patterns for memory]. / Rôle des rythmes cérébraux dans la fonction mnésique du sommeil.

Sleep is crucial for the selective processing and strengthening of information encoded during wakefulness, known as memory consolidation. The different phases of sleep are characterized by specific neuronal activities associated with memory consolidation and homeostatic regulation. In the hippocampus during non-REM sleep, neural patterns called sharp-wave ripple complexes are associated with reactivations of the neural activity that occurred during wakefulness. These reactivations, through their coordinations with cortical slow oscillations and thalamocortical spindles, contribute to the consolidation of spatial memories by strengthening neuronal connections. Cortical slow waves are also a marker of synaptic homeostasis, a regulatory phenomenon maintaining networks in a functional range of firing rates. Finally, REM sleep is also important for memory, although the underlying physiology and the role of theta waves deserves to be further explored.

Title: Rôle des rythmes cérébraux dans la fonction mnésique du sommeil. Abstract: Le sommeil est crucial pour le renforcement sélectif des souvenirs et la régulation des réseaux neuronaux impliqués dans la formation de la mémoire. Ces fonctions sont sous-tendues par des motifs neuraux spécifiques associés aux différentes phases du sommeil. Dans l'hippocampe, les complexes onde aiguë-ondulation du sommeil à ondes lentes sont associés à des réactivations de l'activité neuronale de l'éveil. En se coordonnant avec les ondes lentes et les fuseaux corticaux, ces réactivations contribuent à la consolidation de la mémoire spatiale. Les ondes lentes sont également un marqueur de l'homéostasie synaptique. La physiologie du sommeil paradoxal et des ondes thêta associées reste à explorer.

The role of the hippocampus in the consolidation of emotional memories during sleep.

Episodic memory relies on the hippocampus, a heterogeneous brain region with distinct functions. Spatial representations in the dorsal hippocampus (dHPC) are crucial for contextual memory, while the ventral hippocampus (vHPC) is more involved in emotional processing. Here, we review the literature in rodents highlighting the anatomical and functional properties of the hippocampus along its dorsoventral axis that underlie its role in contextual and emotional memory encoding, consolidation, and retrieval. We propose that the coordination between the dorsal and vHPC through theta oscillations during rapid eye movement (REM) sleep, and through sharp-wave ripples during non-REM (NREM) sleep, might facilitate the transfer of contextual information for integration with valence-related processing in other structures of the network. Further investigation into the physiology of the vHPC and its connections with other brain areas is needed to deepen the current understanding of emotional memory consolidation during sleep.

Brain neural patterns and the memory function of sleep.

Sleep is crucial for healthy cognition, including memory. The two main phases of sleep, REM (rapid eye movement) and non-REM sleep, are associated with characteristic electrophysiological patterns that are recorded using surface and intracranial electrodes. These patterns include sharp-wave ripples, cortical slow oscillations, delta waves, and spindles during non-REM sleep and theta oscillations during REM sleep. They reflect the precisely timed activity of underlying neural circuits. Here, we review how these electrical signatures have been guiding our understanding of the circuits and processes sustaining memory consolidation during sleep, focusing on hippocampal theta oscillations and sharp-wave ripples and how they coordinate with cortical patterns. Finally, we highlight how these brain patterns could also sustain sleep-dependent homeostatic processes and evoke several potential future directions for research on the memory function of sleep.

Reactivations of emotional memory in the hippocampus-amygdala system during sleep.

The consolidation of context-dependent emotional memory requires communication between the hippocampus and the basolateral amygdala (BLA), but the mechanisms of this process are unknown. We recorded neuronal ensembles in the hippocampus and BLA while rats learned the location of an aversive air puff on a linear track, as well as during sleep before and after training. We found coordinated reactivations between the hippocampus and the BLA during non-REM sleep following training. These reactivations peaked during hippocampal sharp wave-ripples (SPW-Rs) and involved a subgroup of BLA cells positively modulated during hippocampal SPW-Rs. Notably, reactivation was stronger for the hippocampus-BLA correlation patterns representing the run direction that involved the air puff than for the 'safe' direction. These findings suggest that consolidation of contextual emotional memory occurs during ripple-reactivation of hippocampus-amygdala circuits.

Hippocampo-cortical coupling mediates memory consolidation during sleep.

Memory consolidation is thought to involve a hippocampo-cortical dialog during sleep to stabilize labile memory traces for long-term storage. However, direct evidence supporting this hypothesis is lacking. We dynamically manipulated the temporal coordination between the two structures during sleep following training on a spatial memory task specifically designed to trigger encoding, but not memory consolidation. Reinforcing the endogenous coordination between hippocampal sharp wave-ripples, cortical delta waves and spindles by timed electrical stimulation resulted in a reorganization of prefrontal cortical networks, along with subsequent increased prefrontal responsivity to the task and high recall performance on the next day, contrary to control rats, which performed at chance levels. Our results provide, to the best of our knowledge, the first direct evidence for a causal role of a hippocampo-cortical dialog during sleep in memory consolidation, and indicate that the underlying mechanism involves a fine-tuned coordination between sharp wave-ripples, delta waves and spindles.

Learning-induced plasticity regulates hippocampal sharp wave-ripple drive.

Hippocampal sharp wave-ripples (SPW-Rs) and associated place-cell reactivations are crucial for spatial memory consolidation during sleep and rest. However, it remains unclear how learning and consolidation requirements influence and regulate subsequent SPW-R activity. Indeed, SPW-R activity has been observed not only following complex behavioral tasks, but also after random foraging in familiar environments, despite markedly different learning requirements. Because transient increases in SPW-R rates have been reported following training on memory tasks, we hypothesized that SPW-R activity following learning (but not routine behavior) could involve specific regulatory processes related to ongoing consolidation. Interfering with ripples would then result in a dynamic compensatory response only when initial memory traces required consolidation. Here we trained rats on a spatial memory task, and showed that subsequent sleep periods where ripple activity was perturbed by timed electrical stimulation were indeed characterized by increased SPW-R occurrence rates compared with control sleep periods where stimulations were slightly delayed in time and did not interfere with ripples. Importantly, this did not occur following random foraging in a familiar environment. We next showed that this dynamic response was abolished following injection of an NMDA receptor blocker (MK-801) before, but not after training. Our results indicate that NMDA receptor-dependent processes occurring during learning, such as network "tagging" and plastic changes, regulate subsequent ripple-mediated consolidation of spatial memory during sleep.

Reversed theta sequences of hippocampal cell assemblies during backward travel.

Hippocampal cell assemblies coding for past, present and future events form theta-timescale (~100 ms) sequences that represent spatio-temporal episodes. However, the underlying mechanisms remain largely unknown. We recorded hippocampal and entorhinal cortical activity as rats experienced backward travel on a model train. Although the firing fields of place cells remained stable, the order in which they were activated in the theta sequence was reversed during backward travel. Thus, hippocampal cell assemblies coordinated their relative timing to correctly predict the sequential traversal of place fields in reverse order. At the single-cell level, theta phase represented distance traveled through the field, even though the head of the rat was oriented opposite to travel direction and entorhinal head-direction cells maintained their preferred firing direction. Our results challenge most theoretical models of theta sequence generation in the hippocampus.

Hippocampal ripples and memory consolidation.

During slow wave sleep and quiet wakefulness, the hippocampus generates high frequency field oscillations (ripples) during which pyramidal neurons replay previous waking activity in a temporally compressed manner. As a result, reactivated firing patterns occur within shorter time windows propitious for synaptic plasticity within the hippocampal network and in downstream neocortical structures. This is consistent with the long-held view that ripples participate in strengthening and reorganizing memory traces, possibly by mediating information transfer to neocortical areas. Recent studies have confirmed that ripples and associated neuronal reactivations play a causal role in memory consolidation during sleep and rest. However, further research will be necessary to better understand the neurophysiological mechanisms of memory consolidation, in particular the selection of reactivated assemblies, and the functional specificity of awake ripples.

Selective suppression of hippocampal ripples impairs spatial memory.

Sharp wave-ripple (SPW-R) complexes in the hippocampus-entorhinal cortex are believed to be important for transferring labile memories from the hippocampus to the neocortex for long-term storage. We found that selective elimination of SPW-Rs during post-training consolidation periods resulted in performance impairment in rats trained on a hippocampus-dependent spatial memory task. Our results provide evidence for a prominent role of hippocampal SPW-Rs in memory consolidation.