State dependent coupling of hippocampal oscillations
- European Brain Research Institute, Italy
- Radboud University Nijmegen, Netherlands
Abstract
Oscillations occurring simultaneously in a given area represent a physiological unit of brain states. They allow for temporal segmentation of spikes and support distinct behaviors. To establish how multiple oscillatory components co-varies simultaneously and influence neuronal firing during sleep and wakefulness in mice, we describe a multi-variate analytical framework for constructing the state space of hippocampal oscillations. Examining the co-occurrence patterns of oscillations on the state space, across species, uncovered the presence of network constraints and distinct set of cross-frequency interactions during wakefulness as compared to sleep. We demonstrated how the state space can be used as a canvas to map the neural firing and found that distinct neurons during navigation were tuned to different sets of simultaneously occurring oscillations during sleep. This multivariate analytical framework provides a window to move beyond classical bivariate pipelines, for investigating oscillations and neuronal firing, thereby allowing to factor-in the complexity of oscillation-population interactions.
Data availability
Datasets used in this study are available at Crcns.org (HC11 dataset) and Donders Repository (https://data.donders.ru.nl/collections/di/dcn/DSC_62002873_05_861)All codes are available made at https://github.com/brijeshmodi12/network_state_space
Article and author information
Author details
Funding
European Union Horizon 2020 research and innovation program MGATE (765549)
- Francesco P Battaglia
European Union Horizon 2020 research and innovation (840704)
- Federico Stella
ERC Advanced Grant (833964)
- Francesco P Battaglia
Telethon (GGP16083)
- Enrico Cherubini
Del Monte Foundation
- Enrico Cherubini
EMBO short term fellowship (8464)
- Brijesh Modi
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Antonio Fernandez-Ruiz, Cornell University, United States
Ethics
Animal experimentation: In compliance with Dutch law and institutional regulations, all animal procedures concerningrecordings from freely moving or sleeping mice were approved by the Central Commissie Dierproeven(CCD) and conducted in accordance with the Experiments on Animals Act (project number 2016-014and protocol numbers 0029).All experiments from head-restrained animals were performed in accordance with the Italian AnimalWelfare legislation (D.L. 26/2014) that implemented the European Committee Council Directive(2010/63 EEC) and were approved by local veterinary authorities, the EBRI ethical committee, andthe Italian Ministry of Health (565/PR18) All efforts were made to minimize animal suffering and toreduce the number of animals used
Version history
- Preprint posted: May 4, 2022 (view preprint)
- Received: May 13, 2022
- Accepted: July 17, 2023
- Accepted Manuscript published: July 18, 2023 (version 1)
- Version of Record published: August 9, 2023 (version 2)
Copyright
© 2023, Modi 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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State dependent coupling of hippocampal oscillations
eLife 12:e80263.
https://doi.org/10.7554/eLife.80263
Further reading
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- Neuroscience
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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- Neuroscience
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.
