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Network models provide insights into how oriens-lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillations.

Ferguson KA, Huh CY, Amilhon B, Manseau F, Williams S, Skinner FK - Front Syst Neurosci (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Division of Fundamental Neurobiology, Toronto Western Research Institute, University Health Network Toronto, ON, Canada ; Department of Physiology, University of Toronto Toronto, ON, Canada.

ABSTRACT
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.

No MeSH data available.


(A) An example trace of the EPSCs recorded from a PV+ interneuron (top) during a network theta oscillation (bottom). The EPSCs were recorded under voltage clamp at −85 mV (junction potential corrected), the inhibitory reversal potential, to eliminate IPSCs. Note that the cell receives large excitatory inputs, that are precisely timed to the peak of the LFP. (B) Same as in (A) but for a SOM+ interneuron. Note the difference in scales: EPSCs received by SOM+ interneurons are smaller than those received by PV+ interneurons.
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Figure 3: (A) An example trace of the EPSCs recorded from a PV+ interneuron (top) during a network theta oscillation (bottom). The EPSCs were recorded under voltage clamp at −85 mV (junction potential corrected), the inhibitory reversal potential, to eliminate IPSCs. Note that the cell receives large excitatory inputs, that are precisely timed to the peak of the LFP. (B) Same as in (A) but for a SOM+ interneuron. Note the difference in scales: EPSCs received by SOM+ interneurons are smaller than those received by PV+ interneurons.

Mentions: EPSCs received by PV+ and SOM+ cells are quite precisely timed with respect to the peak of the LFP (Figure 3). However, to target specifically PV+ or SOM+ interneurons, our voltage clamp recordings were done separately on PV-tdTomato and SOM-tdTomato mice, respectively. Thus, to simulate the effect of simultaneously recorded PV+ and SOM+ EPSC recordings, we developed an algorithm to cut and shift the EPSCs. In this way, the two recordings exhibited EPSCs at the same frequency, and the EPSC peaks aligned (Figure 4). We will refer to these frequency-matched currents as EPSCPV and EPSCOLM, as shown in Figure 5.


Network models provide insights into how oriens-lacunosum-moleculare and bistratified cell interactions influence the power of local hippocampal CA1 theta oscillations.

Ferguson KA, Huh CY, Amilhon B, Manseau F, Williams S, Skinner FK - Front Syst Neurosci (2015)

(A) An example trace of the EPSCs recorded from a PV+ interneuron (top) during a network theta oscillation (bottom). The EPSCs were recorded under voltage clamp at −85 mV (junction potential corrected), the inhibitory reversal potential, to eliminate IPSCs. Note that the cell receives large excitatory inputs, that are precisely timed to the peak of the LFP. (B) Same as in (A) but for a SOM+ interneuron. Note the difference in scales: EPSCs received by SOM+ interneurons are smaller than those received by PV+ interneurons.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4528165&req=5

Figure 3: (A) An example trace of the EPSCs recorded from a PV+ interneuron (top) during a network theta oscillation (bottom). The EPSCs were recorded under voltage clamp at −85 mV (junction potential corrected), the inhibitory reversal potential, to eliminate IPSCs. Note that the cell receives large excitatory inputs, that are precisely timed to the peak of the LFP. (B) Same as in (A) but for a SOM+ interneuron. Note the difference in scales: EPSCs received by SOM+ interneurons are smaller than those received by PV+ interneurons.
Mentions: EPSCs received by PV+ and SOM+ cells are quite precisely timed with respect to the peak of the LFP (Figure 3). However, to target specifically PV+ or SOM+ interneurons, our voltage clamp recordings were done separately on PV-tdTomato and SOM-tdTomato mice, respectively. Thus, to simulate the effect of simultaneously recorded PV+ and SOM+ EPSC recordings, we developed an algorithm to cut and shift the EPSCs. In this way, the two recordings exhibited EPSCs at the same frequency, and the EPSC peaks aligned (Figure 4). We will refer to these frequency-matched currents as EPSCPV and EPSCOLM, as shown in Figure 5.

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Division of Fundamental Neurobiology, Toronto Western Research Institute, University Health Network Toronto, ON, Canada ; Department of Physiology, University of Toronto Toronto, ON, Canada.

ABSTRACT
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.

No MeSH data available.