Interneuronal mechanisms of hippocampal theta oscillation in a full-scale model of the rodent CA1 circuit
- Boston University, United States
- Stanford University, United States
- University of California, Irvine, United States
Abstract
The hippocampal theta rhythm plays important roles in information processing; however, the mechanisms of its generation are not well understood. We developed a data-driven, supercomputer-based, full-scale (1:1) model of the rodent CA1 area and studied its interneurons during theta oscillations. Theta rhythm with phase-locked gamma oscillations and phase-preferential discharges of distinct interneuronal types spontaneously emerged from the isolated CA1 circuit without rhythmic inputs. Perturbation experiments identified parvalbumin-expressing interneurons and neurogliaform cells, as well as interneuronal diversity itself, as important factors in theta generation. These simulations reveal new insights into the spatiotemporal organization of the CA1 circuit during theta oscillations.
Data availability
-
Simulation results from full scale and rationally reduced network models of the isolated hippocampal CA1 subfield in ratPublicly available at the Open Science Framework.
-
Hippocampal CA1 network in parallel NEURON with spontaneous theta, gamma: full scale & network clampPublicly available at SenseLab (accession no: 187604).
-
Firing pattern of O-LM cells in mouse hippocampal CA1.Publicly available at the Open Science Framework.
-
Intracellular, in vitro somatic membrane potential recordings from whole cell patch clamped rodent hippocampal CA1 neurons.Publicly available at the Open Science Framework.
Article and author information
Author details
Marianne J Bezaire
Funding
National Institutes of Health (NS35915)
- Ivan Soltesz
National Science Foundation (IOS-1310378)
- Ivan Soltesz
National Institutes of Health (F32NS090753)
- Marianne J Bezaire
National Science Foundation (DGE-0808392)
- Marianne J Bezaire
NSF XSEDE Allocations (TG-IBN140007,TG-IBN130022,TG-IBN100011)
- Marianne J Bezaire
- Ivan Raikov
- Ivan Soltesz
National Institutes of Health (NS090583)
- Ivan Soltesz
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Frances K Skinner, University Health Network, Canada
Version history
- Received: June 12, 2016
- Accepted: December 15, 2016
- Accepted Manuscript published: December 23, 2016 (version 1)
- Version of Record published: February 16, 2017 (version 2)
Copyright
© 2016, Bezaire 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
-
- 6,494
- views
-
- 1,398
- downloads
-
- 173
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
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)
Interneuronal mechanisms of hippocampal theta oscillation in a full-scale model of the rodent CA1 circuit
eLife 5:e18566.
https://doi.org/10.7554/eLife.18566
Further reading
-
- Computational and Systems Biology
Interacting molecules create regulatory architectures that can persist despite turnover of molecules. Although epigenetic changes occur within the context of such architectures, there is limited understanding of how they can influence the heritability of changes. Here, I develop criteria for the heritability of regulatory architectures and use quantitative simulations of interacting regulators parsed as entities, their sensors, and the sensed properties to analyze how architectures influence heritable epigenetic changes. Information contained in regulatory architectures grows rapidly with the number of interacting molecules and its transmission requires positive feedback loops. While these architectures can recover after many epigenetic perturbations, some resulting changes can become permanently heritable. Architectures that are otherwise unstable can become heritable through periodic interactions with external regulators, which suggests that mortal somatic lineages with cells that reproducibly interact with the immortal germ lineage could make a wider variety of architectures heritable. Differential inhibition of the positive feedback loops that transmit regulatory architectures across generations can explain the gene-specific differences in heritable RNA silencing observed in the nematode Caenorhabditis elegans. More broadly, these results provide a foundation for analyzing the inheritance of epigenetic changes within the context of the regulatory architectures implemented using diverse molecules in different living systems.
-
- Computational and Systems Biology
- Ecology
Collaborative hunting, in which predators play different and complementary roles to capture prey, has been traditionally believed to be an advanced hunting strategy requiring large brains that involve high-level cognition. However, recent findings that collaborative hunting has also been documented in smaller-brained vertebrates have placed this previous belief under strain. Here, using computational multi-agent simulations based on deep reinforcement learning, we demonstrate that decisions underlying collaborative hunts do not necessarily rely on sophisticated cognitive processes. We found that apparently elaborate coordination can be achieved through a relatively simple decision process of mapping between states and actions related to distance-dependent internal representations formed by prior experience. Furthermore, we confirmed that this decision rule of predators is robust against unknown prey controlled by humans. Our computational ecological results emphasize that collaborative hunting can emerge in various intra- and inter-specific interactions in nature, and provide insights into the evolution of sociality.
