Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks
- Universidad Miguel Hernández, Spain
- Universitat Politècnica de València, Spain
- Cajal Institute, Spain
- Universidad de La Laguna, Spain
- Universitat de les Illes Balears, Spain
- Instituto de Neurociencias, Consejo Superior de Investigaciones Científicas and Universidad Miguel Hernández, Spain
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
Víctor J López-Madrona
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.
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).
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.
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Different theta frameworks coexist in the rat hippocampus and are coordinated during memory-guided and novelty tasks
eLife 9:e57313.
https://doi.org/10.7554/eLife.57313
Further reading
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The basolateral amygdala (BLA) is a key site where fear learning takes place through synaptic plasticity. Rodent research shows prominent low theta (~3–6 Hz), high theta (~6–12 Hz), and gamma (>30 Hz) rhythms in the BLA local field potential recordings. However, it is not understood what role these rhythms play in supporting the plasticity. Here, we create a biophysically detailed model of the BLA circuit to show that several classes of interneurons (PV, SOM, and VIP) in the BLA can be critically involved in producing the rhythms; these rhythms promote the formation of a dedicated fear circuit shaped through spike-timing-dependent plasticity. Each class of interneurons is necessary for the plasticity. We find that the low theta rhythm is a biomarker of successful fear conditioning. The model makes use of interneurons commonly found in the cortex and, hence, may apply to a wide variety of associative learning situations.
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