Cortico-Hippocampal Oscillations Are Associated With the Developmental Onset of Hippocampal-Dependent Memory

Abstract

Hippocampal-dependent memories emerge late during postnatal development, aligning with hippocampal maturation. During sleep, the two-stage memory formation model states that through hippocampal-neocortical interactions, cortical slow-oscillations (SO), thalamocortical Spindles, and hippocampal sharp-wave ripples (SWR) are synchronized, allowing for the consolidation of hippocampal-dependent memories. However, evidence supporting this hypothesis during development is still lacking. Therefore, we performed successive object-in-place tests during a window of memory emergence and recorded in vivo the occurrence of SO, Spindles, and SWR during sleep, immediately after the memory encoding stage of the task. We found that hippocampal-dependent memory emerges at the end of the 4th postnatal week independently of task overtraining. Furthermore, we observed that those animals with better performance in the memory task had increased Spindle density and duration and lower density of SWR. Moreover, we observed changes in the SO-Spindle and Spindle-SWR temporal-coupling during this developmental period. Our results provide new evidence for the onset of hippocampal-dependent memory and its relationship to the oscillatory phenomenon occurring during sleep that helps us understand how memory consolidation models fit into the early stages of postnatal development.

A classification-based generative approach to selective targeting of global slow oscillations during sleep

“…Oscillatory events found in the EEG during NREM sleep have been causally implicated in changes in overnight memory performance. Cortical slow oscillations (SOs, 0.5−1.5 Hz), thalamo-cortical spindles (11−16 Hz) and hippocampal sharp-wave ripples (>100Hz) ( Mölle and Born, 2011 ; Binder et al, 2014 ; Brancaccio et al, 2020 ; Azimi et al, 2021 ; Abdellahi et al, 2023 ), have all been experimentally connected to consolidation of episodic memory, with performance benefitting from enhancement of the oscillations and their coordination, or disruption of these oscillations leading to loss of performance ( Muehlroth et al, 2019 ; Aksamaz et al, 2022 ; Bastian et al, 2022 ; García-Pérez et al, 2022 ). The current mechanistic understanding of the role these oscillations play in memory changes centers on their time-based coordination, with hierarchical nesting of ripples within spindles, and in turn within SOs, hypothesized to support reactivation of memory traces, and hence mediate the activity-dependent reorganization of synaptic connections that strengthen episodic memory [known as Active Systems Consolidation Theory ( Klinzing et al, 2019 ; Mason et al, 2021 )].…”

A Classification-Based Generative Approach to Selective Targeting of Global Slow Oscillations during Sleep

“…Oscillatory events found in the EEG during NREM sleep have been causally implicated in changes in overnight memory performance. Cortical slow oscillations (SOs, 0.5-1.5 Hz), thalamo-cortical spindles (11)(12)(13)(14)(15)(16) and hippocampal sharp-wave ripples (>100Hz) [5,6], have all been experimentally connected to consolidation of episodic memory, with performance benefitting from enhancement of the oscillations and their coordination, or disruption of these oscillations leading to loss of performance [7][8][9][10]. The current mechanistic understanding of the role these oscillations play in memory changes centers on their time-based coordination, with hierarchical nesting of ripples within spindles, and in turn within SOs, hypothesized to support reactivation of memory traces, and hence mediate the activity-dependent reorganization of synaptic connections that strengthen episodic memory (known as Active Systems Consolidation Theory [11,12]).…”

A scoping review of the relationship between alcohol, memory consolidation and ripple activity: An overview of common methodologies to analyse ripples

“…Several biomarkers for cognitive operations in the hippocampus have been studied, including altered structure, functional connectivity and volume of the hippocampus (Feng et al, 2019); however, in this review; we concentrate on sharp wave–ripple (SWR) complexes. SWRs are events that occur during non‐rapid‐eye movement sleep and ‘off‐line’ states of the brain associated with consummatory behaviours and memory consolidation (Buzsáki, 2015; Cowen et al, 2020; García‐Pérez et al, 2022; Oliva et al, 2020; Zhen et al, 2021). They indicate the reactivation of neural sequences through the simultaneous presence of two connected yet distinct events: a pronounced deflection in the local field potential called sharp wave and a rapid oscillation referred to as ripple (Buzsáki et al, 1992; Ylinen et al, 1995).…”