Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks
Abstract
Hippocampal firing is organized in theta sequences controlled by internal memory processes and by external sensory cues, but how these computations are coordinated is not fully understood. Although theta activity is commonly studied as a unique coherent oscillation, it is the result of complex interactions between different rhythm generators. Here, by separating hippocampal theta activity in three different current generators, we found epochs with variable theta frequency and phase coupling, suggesting flexible interactions between theta generators. We found that epochs of highly synchronized theta rhythmicity preferentially occurred during behavioral tasks requiring coordination between internal memory representations and incoming sensory information. In addition, we found that gamma oscillations were associated with specific theta generators and the strength of theta-gamma coupling predicted the synchronization between theta generators. We propose a mechanism for segregating or integrating hippocampal computations based on the flexible coordination of different theta frameworks to accommodate the cognitive needs.
Data availability
All datasets are available at: http://dx.doi.org/10.20350/digitalCSIC/12537
Article and author information
Author details
Funding
European Regional Development Fund (BFU2015-64380-C2-1-R)
- Santiago Canals
European Regional Development Fund (BFU2015-64380-C2-2-R)
- David Moratal
European Regional Development Fund (PGC2018-101055-B-I00)
- Santiago Canals
Horizon 2020 Framework Programme (668863 (SyBil-AA))
- Santiago Canals
Spanish State Research Agency (SEV- 2017-0723)
- Santiago Canals
MINECO (TEC2016-80063-C3-3-R)
- Claudio R Mirasso
MINECO (TEC2016-80063-C3-2-R)
- Ernesto Pereda
Spanish State Research Agency (MDM-2017-0711)
- Claudio R Mirasso
MINECO (SAF2016-80100-R)
- Oscar Herreras
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Martin Vinck, Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Germany
Ethics
Animal experimentation: All animal experiments were approved by the Animal Care and Use Committee of the Instituto de Neurociencias de Alicante, Alicante, Spain, and comply with the Spanish (law 32/2007) and European regulations (EU directive 86/609, EU decree 2001-486, and EU recommendation 2007/526/EC).
Version history
- Received: March 27, 2020
- Accepted: July 19, 2020
- Accepted Manuscript published: July 20, 2020 (version 1)
- Accepted Manuscript updated: July 22, 2020 (version 2)
- Version of Record published: August 7, 2020 (version 3)
Copyright
© 2020, López-Madrona 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.
Metrics
-
- 4,829
- Page views
-
- 639
- Downloads
-
- 39
- Citations
Article citation count generated by polling the highest count across the following sources: Scopus, PubMed Central, Crossref.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.
-
- Medicine
- Neuroscience
In recent years, there has been debate about the effectiveness of treatments from different fields, such as neurostimulation, neurofeedback, brain training, and pharmacotherapy. This debate has been fuelled by contradictory and nuanced experimental findings. Notably, the effectiveness of a given treatment is commonly evaluated by comparing the effect of the active treatment versus the placebo on human health and/or behaviour. However, this approach neglects the individual’s subjective experience of the type of treatment she or he received in establishing treatment efficacy. Here, we show that individual differences in subjective treatment - the thought of receiving the active or placebo condition during an experiment - can explain variability in outcomes better than the actual treatment. We analysed four independent datasets (N = 387 participants), including clinical patients and healthy adults from different age groups who were exposed to different neurostimulation treatments (transcranial magnetic stimulation: Studies 1 and 2; transcranial direct current stimulation: Studies 3 and 4). Our findings show that the inclusion of subjective treatment can provide a better model fit either alone or in interaction with objective treatment (defined as the condition to which participants are assigned in the experiment). These results demonstrate the significant contribution of subjective experience in explaining the variability of clinical, cognitive, and behavioural outcomes. We advocate for existing and future studies in clinical and non-clinical research to start accounting for participants’ subjective beliefs and their interplay with objective treatment when assessing the efficacy of treatments. This approach will be crucial in providing a more accurate estimation of the treatment effect and its source, allowing the development of effective and reproducible interventions.