Oscillations support short latency co-firing of neurons during human episodic memory formation
- University of Birmingham, United Kingdom
- Queen Elizabeth Hospital Birmingham, United Kingdom
- University Hospital Erlangen, Germany
- University of Glasgow, United Kingdom
- Netherlands Institute for Neuroscience, Netherlands
Abstract
Theta and gamma oscillations in the medial temporal lobe are suggested to play a critical role for human memory formation via establishing synchrony in neural assemblies. Arguably, such synchrony facilitates efficient information transfer between neurons and enhances synaptic plasticity, both of which benefit episodic memory formation. However, to date little evidence exists from humans that would provide direct evidence for such a specific role of theta and gamma oscillations for episodic memory formation. Here we investigate how oscillations shape the temporal structure of neural firing during memory formation in the medial temporal lobe. We measured neural firing and local field potentials in human epilepsy patients via micro-wire electrode recordings to analyze whether brain oscillations are related to co-incidences of firing between neurons during successful and unsuccessful encoding of episodic memories. The results show that phase-coupling of neurons to faster theta and gamma oscillations correlates with co-firing at short latencies (~20-30 ms) and occurs during successful memory formation. Phase-coupling at slower oscillations in these same frequency bands, in contrast, correlates with longer co-firing latencies and occurs during memory failure. Thus, our findings suggest that neural oscillations play a role for the synchronization of neural firing in the medial temporal lobe during the encoding of episodic memories.
Data availability
All code used for data analysis and visualization of results is deposited here: https://osf.io/fngz8/
Article and author information
Author details
Bernhard P Staresina
Funding
European Research Council (647954)
- Simon Hanslmayr
Economic and Social Research Council (ES/R010072/1)
- Simon Hanslmayr
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Lucia Melloni, Max Planck Institute for Empirical Aesthetics, Germany
Ethics
Human subjects: Informed consent to participate in the experiments and consent to publish the results was obtained from the patients prior to data collection. Ethical approvals were given by National Research Ethics Service (NRES), Research Ethics Committee (Nr. 15/WM/0219), the ethical review board of the Friedrich-Alexander Universität Erlangen-Nürnberg (Nr. 124_12 B), and the Medical Ethical Review board of the Vrije Universiteit Medisch Centrum (Nr. NL55554.029.15), for Birmingham, Erlangen and Amsterdam respectively.
Version history
- Preprint posted: January 28, 2021 (view preprint)
- Received: February 23, 2022
- Accepted: November 29, 2022
- Accepted Manuscript published: November 30, 2022 (version 1)
- Version of Record published: December 8, 2022 (version 2)
Copyright
© 2022, Roux et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Oscillations support short latency co-firing of neurons during human episodic memory formation
eLife 11:e78109.
https://doi.org/10.7554/eLife.78109
Further reading
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Asymmetries in the size of structures deep below the cortex explain how alpha oscillations in the brain respond to shifts in attention.
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Evidence suggests that subcortical structures play a role in high-level cognitive functions such as the allocation of spatial attention. While there is abundant evidence in humans for posterior alpha band oscillations being modulated by spatial attention, little is known about how subcortical regions contribute to these oscillatory modulations, particularly under varying conditions of cognitive challenge. In this study, we combined MEG and structural MRI data to investigate the role of subcortical structures in controlling the allocation of attentional resources by employing a cued spatial attention paradigm with varying levels of perceptual load. We asked whether hemispheric lateralization of volumetric measures of the thalamus and basal ganglia predicted the hemispheric modulation of alpha-band power. Lateral asymmetry of the globus pallidus, caudate nucleus, and thalamus predicted attention-related modulations of posterior alpha oscillations. When the perceptual load was applied to the target and the distractor was salient caudate nucleus asymmetry predicted alpha-band modulations. Globus pallidus was predictive of alpha-band modulations when either the target had a high load, or the distractor was salient, but not both. Finally, the asymmetry of the thalamus predicted alpha band modulation when neither component of the task was perceptually demanding. In addition to delivering new insight into the subcortical circuity controlling alpha oscillations with spatial attention, our finding might also have clinical applications. We provide a framework that could be followed for detecting how structural changes in subcortical regions that are associated with neurological disorders can be reflected in the modulation of oscillatory brain activity.
