High frequency oscillations in human memory and cognition: a neurophysiological substrate of engrams?

• Published in: Brain (London, England : 1878) Vol. 147; no. 9; pp. 2966 - 2982
• Main Authors: Kucewicz, Michal T, Cimbalnik, Jan, Garcia-Salinas, Jesus S, Brazdil, Milan, Worrell, Gregory A
• Format: Journal Article
• Language: English
• Published: UK Oxford University Press 03.09.2024
• Subjects: Brain - physiology; Brain Waves - physiology; Cognition - physiology; Electroencephalography; Humans; Memory - physiology; Review; local field potential; network oscillations; cognition; memory consolidation; sharp-wave ripples; intracranial EEG
• ISSN: 0006-8950; 1460-2156; 1460-2156
• DOI: 10.1093/brain/awae159

Abstract Despite advances in understanding the cellular and molecular processes underlying memory and cognition, and recent successful modulation of cognitive performance in brain disorders, the neurophysiological mechanisms remain underexplored. High frequency oscillations beyond the classic electroencephalogram spectrum have emerged as a potential neural correlate of fundamental cognitive processes. High frequency oscillations are detected in the human mesial temporal lobe and neocortical intracranial recordings spanning gamma/epsilon (60–150 Hz), ripple (80–250 Hz) and higher frequency ranges. Separate from other non-oscillatory activities, these brief electrophysiological oscillations of distinct duration, frequency and amplitude are thought to be generated by coordinated spiking of neuronal ensembles within volumes as small as a single cortical column. Although the exact origins, mechanisms and physiological roles in health and disease remain elusive, they have been associated with human memory consolidation and cognitive processing. Recent studies suggest their involvement in encoding and recall of episodic memory with a possible role in the formation and reactivation of memory traces. High frequency oscillations are detected during encoding, throughout maintenance, and right before recall of remembered items, meeting a basic definition for an engram activity. The temporal coordination of high frequency oscillations reactivated across cortical and subcortical neural networks is ideally suited for integrating multimodal memory representations, which can be replayed and consolidated during states of wakefulness and sleep. High frequency oscillations have been shown to reflect coordinated bursts of neuronal assembly firing and offer a promising substrate for tracking and modulation of the hypothetical electrophysiological engram.Kucewicz et al. review the role of high frequency gamma and ripple oscillations in human memory and cognition, and propose that these fast activity bursts track coordinated firing of neuronal assemblies across the brain during the formation and recall of memory traces.