Ripples in the medial temporal lobe are relevant for human memory consolidation

Abstract

High-frequency oscillations (ripples) have been described in the hippocampus and rhinal cortex of both animals and human subjects and have been linked to replay and consolidation of previously acquired information. More specifically, studies in rodents suggested that ripples are generated in the hippocampus and are then transferred into the rhinal cortex, and that they occur predominantly during negative half waves of neocortical slow oscillations. Recordings in human epilepsy patients used either microelectrodes or foramen ovale electrodes; it is thus unclear whether macroelectrodes, which are routinely used for pre-surgical investigations, allow the recording of ripples as well. Furthermore, no direct link between ripples and behavioural performance has yet been established. Here, we recorded intracranial electroencephalogram with macroelectrodes from the hippocampus and rhinal cortex contralateral to the seizure onset zone in 11 epilepsy patients during a memory consolidation task while they were having an afternoon 'nap', i.e. a sleep period of approximately 1 h duration. We found that ripples could reliably be detected both in the hippocampus and in the rhinal cortex and had a similar frequency composition to events recorded previously with microelectrodes in humans. Results from cross-correlation analysis revealed that hippocampal events were closely locked to rhinal events and were consistent with findings on transmission of ripples from the hippocampus into the rhinal cortex. Furthermore, hippocampal ripples were significantly locked to the phase of hippocampal delta band activity, which might provide a mechanism for the reported phase-locking to neocortical slow oscillations. Ripples occurred with the highest incidence during periods when subjects lay awake during the nap time. Finally, we found that the number of rhinal, but not hippocampal, ripples was correlated with the number of successfully recalled items (post-nap) learned prior to sleep. These data confirm previous recordings in animals and humans, but move beyond them in several respects: they are the first recordings of ripples in humans during a cognitive task and suggest that ripples are indeed related to behavioural performance; furthermore, they propose a mechanism for phase-locking of ripples to neocortical slow waves via phase coupling to hippocampal delta activity; finally, they show that ripples can be recorded reliably with standard macroelectrodes in the human brain.

High-frequency changes during interictal spikes detected by time-frequency analysis

“…First physiological events are not described to co-occur with epileptic spikes. Second in the mesial temporal structures they are mainly seen during memory consolidation in sleep (Axmacher et al, 2008) and not during wakefulness; in the neocortex they have been mainly described in primary motor and sensory regions (Ball et al, 2008;Curio, 1999), which were not targeted in this study.…”

Spontaneous default network activity reflects behavioral variability independent of mind-wandering

“…Simultaneous electrophysiology with fMRI suggests that spontaneous hippocampal ripples are followed by selective activation of the DMN (46). Hippocampal ripples after learning have been shown to be predictive of subsequent memory performance (47). States of mindwandering often involve rehearsal of learned information to prepare for the future.…”

Learning-Induced Plasticity Regulates Hippocampal Sharp Wave-Ripple Drive

“…Similarly, replay of awake neural patterns can be observed even in overtrained animals performing simple routine behaviors that are not expected to require consolidation. However, the rate of SPW-R and associated replay were shown to be increased by experimental induction of synaptic plasticity (Buzsáki, 1984;Behrens et al, 2005), as well as training on a learning task (Kudrimoti et al, 1999;Axmacher et al, 2008;Ramadan et al, 2009). The incidence of SPW-Rs and replay events could therefore constitute an important factor of effective consolidation.…”