The Yin and Yang of Memory Consolidation: Hippocampal and Neocortical

Abstract

While hippocampal and cortical mechanisms of memory consolidation have long been studied, their interaction is poorly understood. We sought to investigate potential interactions with respect to trace dominance, strengthening, and interference associated with postencoding novelty or sleep. A learning procedure was scheduled in a watermaze that placed the impact of novelty and sleep in opposition. Distinct behavioural manipulations—context preexposure or interference during memory retrieval—differentially affected trace dominance and trace survival, respectively. Analysis of immediate early gene expression revealed parallel up-regulation in the hippocampus and cortex, sustained in the hippocampus in association with novelty but in the cortex in association with sleep. These findings shed light on dynamically interacting mechanisms mediating the stabilization of hippocampal and neocortical memory traces. Hippocampal memory traces followed by novelty were more dominant by default but liable to interference, whereas sleep engaged a lasting stabilization of cortical traces and consequent trace dominance after preexposure.

Sharp-wave ripples as a signature of hippocampal-prefrontal reactivation for memory during sleep and waking states

“…Subsequent to these processes during waking states, reactivation during NREM sleep after behavior can support further consolidation of these memories. In particular, it has been proposed that different related memories need to be integrated into "memory schema" to represent associative structures among these memories, which crucially relies on hippocampal-prefrontal interactions (Frankland and Bontempi, 2005;Tse et al, 2007;Lewis and Durrant, 2011;Tse et al, 2011;Battaglia et al, 2012;Genzel et al, 2017;Schlichting and Frankland, 2017). Building on the idea that overlapping reactivation of learned information promotes building memory schema during sleep (Lewis and Durrant, 2011;Feld and Born, 2017), it is tempting to speculate that hippocampal sleep reactivation, followed by prefrontal spindles and delta waves, facilitates the integration of several distinct experiences in the PFC, which therefore manifests as "noisy" reactivation of the most recent experience (Battaglia et al, 2012;Roumis and Frank, 2015;Tang et al, 2017).…”

Atypicalities in sleep and semantic consolidation in autism

“…Sleep spindles are thalamically generated during non‐rapid eye movement (NREM) sleep, and are proposed to support consolidation via their temporal synchrony with hippocampal sharp‐wave ripples and neocortical slow oscillations (Antony, Schönauer, Staresina, & Cairney, ; Diekelmann & Born, ; Genzel et al, ; Latchoumane, Ngo, Born, & Shin, ; Staresina et al, ). It has been hypothesized that spindle‐orchestrated ‘replaying’ patterns of hippocampal and neocortical activity following learning are key to the ‘whole‐brain reorganization’ required for cellular consolidation across distributed neocortical connections (i.e., systems consolidation; Genzel et al, ; see Runyan, Moore, & Dash, , for a review). Sleep spindles have been shown to occur more frequently after learning, and have been associated with synaptic plasticity and improved retention (Muller et al, ; Rosanova & Ulrich, ).…”

Stress early in life leads to cognitive impairments, reduced numbers of CA3 neurons and altered maternal behavior in adult female mice

“…The hippocampus is a crucial part of the limbic system and plays a role both in the cognitive processing such as memory consolidation and retrieval and in the regulation of anxiety, emotional memory and responses to stress. [17][18][19][20] The hippocampus develops during the fetal period in both rodents and humans 21,22 ; however, synaptogenesis and the establishment of enduring connectivity patterns continue for weeks after birth in rodents and for years in humans. 23 In rodents, the first postnatal weeks are crucial for hippocampal development: this is the period when neuronal birth, differentiation and migration are taking place.…”