Network models provide insights into how oriens–lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillations
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)...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2015-08-01
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| Series: | Frontiers in Systems Neuroscience |
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| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fnsys.2015.00110/full |
| _version_ | 1818415872276955136 |
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| author | Katie A Ferguson Katie A Ferguson Carey Y. L. Huh Bénédicte eAmilhon Frédéric eManseau Sylvain eWilliams Frances K Skinner Frances K Skinner |
| author_facet | Katie A Ferguson Katie A Ferguson Carey Y. L. Huh Bénédicte eAmilhon Frédéric eManseau Sylvain eWilliams Frances K Skinner Frances K Skinner |
| author_sort | Katie A Ferguson |
| collection | DOAJ |
| description | 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 a number of OLM-BiC connections and connection strengths.We found that our models operate in regimes in which 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 power of network theta oscillations. Our network models reveal a dynamic interplay between different classes of interneurons in influencing local theta power. |
| first_indexed | 2024-12-14T11:41:53Z |
| format | Article |
| id | doaj.art-23b650b07fbc44068a1a353f49f28e89 |
| institution | Directory Open Access Journal |
| issn | 1662-5137 |
| language | English |
| last_indexed | 2024-12-14T11:41:53Z |
| publishDate | 2015-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Systems Neuroscience |
| spelling | doaj.art-23b650b07fbc44068a1a353f49f28e892022-12-21T23:02:47ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372015-08-01910.3389/fnsys.2015.00110145626Network models provide insights into how oriens–lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillationsKatie A Ferguson0Katie A Ferguson1Carey Y. L. Huh2Bénédicte eAmilhon3Frédéric eManseau4Sylvain eWilliams5Frances K Skinner6Frances K Skinner7Toronto Western Research InstituteUniversity of TorontoDouglas Mental Health University Institute, McGill UniversityDouglas Mental Health University Institute, McGill UniversityDouglas Mental Health University Institute, McGill UniversityDouglas Mental Health University Institute, McGill UniversityToronto Western Research InstituteUniversity of TorontoHippocampal 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 a number of OLM-BiC connections and connection strengths.We found that our models operate in regimes in which 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 power of network theta oscillations. Our network models reveal a dynamic interplay between different classes of interneurons in influencing local theta power.http://journal.frontiersin.org/Journal/10.3389/fnsys.2015.00110/fullSomatostatincomputational modelinhibitioninterneuronRhythmoptogenetics |
| spellingShingle | Katie A Ferguson Katie A Ferguson Carey Y. L. Huh Bénédicte eAmilhon Frédéric eManseau Sylvain eWilliams Frances K Skinner Frances K Skinner Network models provide insights into how oriens–lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillations Frontiers in Systems Neuroscience Somatostatin computational model inhibition interneuron Rhythm optogenetics |
| title | Network models provide insights into how oriens–lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillations |
| title_full | Network models provide insights into how oriens–lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillations |
| title_fullStr | Network models provide insights into how oriens–lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillations |
| title_full_unstemmed | Network models provide insights into how oriens–lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillations |
| title_short | Network models provide insights into how oriens–lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillations |
| title_sort | network models provide insights into how oriens lacunosum moleculare and bistratified cell interactions influence the power of local hippocampal ca1 theta oscillations |
| topic | Somatostatin computational model inhibition interneuron Rhythm optogenetics |
| url | http://journal.frontiersin.org/Journal/10.3389/fnsys.2015.00110/full |
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