Network models provide insights into how oriens-lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillations
Open accessAbstract
Hippocampal theta is a 4-12 Hz rhythm associated with episodic memory, and although it has been studied extensively, the cellular mechanisms underlying its generation are unclear. The complex interactions between different interneuron types, such as those between oriens-lacunosum-moleculare (OLM) interneurons and bistratified cells (BiCs), make their contribution to network rhythms difficult to determine experimentally. We created network models that are tied to experimental work at both cellular and network levels to explore how these interneuron interactions affect the power of local oscillations. Our cellular models were constrained with properties from patch clamp recordings in the CA1 region of an intact hippocampus preparation in vitro. Our network models are composed of three different types of interneurons: parvalbumin-positive (PV+) basket and axo-axonic cells (BC/AACs), PV+ BiCs, and somatostatin-positive OLM cells. Also included is a spatially extended pyramidal cell model to allow for a simplified local field potential representation, as well as experimentally-constrained, theta frequency synaptic inputs to the interneurons. The network size, connectivity, and synaptic properties were constrained with experimental data. To determine how the interactions between OLM cells and BiCs could affect local theta power, we explored how the number of OLM-BiC connections and connection strength affected local theta power. We found that our models operate in regimes that could be distinguished by whether OLM cells minimally or strongly affected the power of network theta oscillations due to balances that, respectively, allow compensatory effects or not. Inactivation of OLM cells could result in no change or even an increase in theta power. We predict that the dis-inhibitory effect of OLM cells to BiCs to pyramidal cell interactions plays a critical role in the resulting power of network theta oscillations. Overall, our network models reveal a dynamic interplay between different classes of interneurons in influencing local theta power.
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GABAergic interneurons, especially the PV+ subtype, play an important role in the regulation of neuronal oscillations in the brain.
“GABAergic interneurons, especially the PV+ subtype, play an important role in the regulation of neuronal oscillations in the brain (24–27) and have also been implicated in neuropsychiatric disease (66; 67).”
From Perineuronal nets, inhibitory interneurons and anxiety-related ventral hippocampal neuronal oscillations are altered by early life adversity (2019) · cites this paper as [26]
The model's interneuronal phase preferences were in line with recent data from the isolated CA1 preparation in vitro, which showed that cells belonging to the broadly defined SOM+ and PV+ classes displayed phase preferences similar to the O-LM, PV+ basket and bistratified cells in the model.
“These results were in line with recent data from the isolated CA1 preparation in vitro (Ferguson et al., 2015) which showed that cells belonging to the broadly defined SOM+ and PV+ classes (identified using genetic drivers) displayed phase preferences similar to the O-LM, PV+ basket and bistratified cells in our model”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Ferguson et al., 2015
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- Authors
- Ferguson, K. A., Huh, C. Y. L., Amilhon, B., Manseau, F., Williams, S., & Skinner, F. K.
- Affiliations
- University Health Network (CA)
- Douglas Mental Health University Institute (CA)
- Corresponding author
- Ferguson, Katie A.
- ORCID
- Venue
- Frontiers in Systems Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2015-08-07
- Volume
- 9
- Pages
- 110-110
- ISSN
- 1662-5137 (ISSN-L)
- PMC
- PMC4528165
- OpenAlex
- W1492234993
- Cited by
- 33
- References
- 59
- Citations by year
- 2025: 2 · 2023: 4 · 2022: 3 · 2021: 3 · 2020: 3 · 2019: 8 · 2018: 4 · 2017: 3 · 2016: 1 · 2015: 2
- FWCI
- 2.01
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Systems Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Compute Canada
- Government of Ontario
- University of Toronto
- Canadian Institutes of Health Research
- Natural Sciences and Engineering Research Council of Canada
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- hippocampal theta oscillations, CA1, oriens-lacunosum moleculare interneurons, network models, local field potentials, parvalbumin interneurons, axo-axonic cells, basket cells, somatostatin interneurons, pyramidal neurons, theta power, synaptic connectivity
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