Integration of Within-Cell Experimental Data With Multi-Compartmental Modeling Predicts H-Channel Densities and Distributions in Hippocampal OLM Cells

Sekulić, Vladislav; Yi, Feng; Garrett, Tavita; Guet-McCreight, Alexandre; Lawrence, J. Josh; Skinner, Frances K.

doi:10.3389/fncel.2020.00277

Cited by 11 publications

(32 citation statements)

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“…However, naturalistic patterns of -mediated IPSPs are likely to impact postsynaptic target cells differently depending on their membrane time constant and resonance properties 86 , 87 . In multi-compartmental models of O-LM cells, IPSPs readily generate theta resonance in part through hyperpolarization-induced recruitment of HCN channels 86 , 88 , 89 , supporting the idea that rhythmic disinhibition via phasic transmission contributes to theta rhythm generation 90 . Due to the fact that O-LM cells have relatively long membrane time constants 35 , bursts of IPSPs at gamma frequency are likely to be integrated, with a burst of depression-resistant IPSPs at gamma frequency to be effective in driving hyperpolarization-induced activation of HCN channels, rebound spikes, and inducing synchronous disinhibition of hippocampal principal cells 19 .…”

Section: Discussionmentioning

confidence: 71%

Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression

Garrett

Deisseroth

et al. 2021

Sci Rep

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Parvalbumin-containing projection neurons of the medial-septum-diagonal band of Broca ($$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB ) are essential for hippocampal rhythms and learning operations yet are poorly understood at cellular and synaptic levels. We combined electrophysiological, optogenetic, and modeling approaches to investigate $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB neuronal properties. $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB neurons had intrinsic membrane properties distinct from acetylcholine- and somatostatin-containing MS-DBB subtypes. Viral expression of the fast-kinetic channelrhodopsin ChETA-YFP elicited action potentials to brief (1–2 ms) 470 nm light pulses. To investigate $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB transmission, light pulses at 5–50 Hz frequencies generated trains of inhibitory postsynaptic currents (IPSCs) in CA1 stratum oriens interneurons. Using a similar approach, optogenetic activation of local hippocampal PV ($$\hbox {PV}_{\text{HC}}$$ PV HC ) neurons generated trains of $$\hbox {PV}_{\text{HC}}$$ PV HC -mediated IPSCs in CA1 pyramidal neurons. Both synapse types exhibited short-term depression (STD) of IPSCs. However, relative to $$\hbox {PV}_{\text{HC}}$$ PV HC synapses, $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB synapses possessed lower initial release probability, transiently resisted STD at gamma (20–50 Hz) frequencies, and recovered more rapidly from synaptic depression. Experimentally-constrained mathematical synapse models explored mechanistic differences. Relative to the $$\hbox {PV}_{\text{HC}}$$ PV HC model, the $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB model exhibited higher sensitivity to calcium accumulation, permitting a faster rate of calcium-dependent recovery from STD. In conclusion, resistance of $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB synapses to STD during short gamma bursts enables robust long-range GABAergic transmission from MS-DBB to hippocampus.

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Section: Discussionmentioning

confidence: 71%

Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression

Garrett

Deisseroth

et al. 2021

Sci Rep

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“…The models upon which the present work is based have been previously published. Detailed descriptions of these models with equations and parameter values can be accessed from Guet-McCreight and Skinner (33) and Sekulic et al (27). Here we provide a brief description:…”

Section: Methodsmentioning

confidence: 99%

“…Two detailed multi-compartment OLM cell models, cell 1 and cell 2, were developed in NEURON (34) using a “neuron-to-model matched” (NMM) approach (27). That is, the morphology, passive properties and h-channel characteristics in each model were specific to cell 1 or 2 as measured in the biological OLM cell, and other biophysical currents were optimized using electrophysiological data specific to cell 1 or 2.…”

Section: Methodsmentioning

confidence: 99%

“…It was found that there is a shift in spike resonance from high to low theta frequencies if, respectively, dendritic h-channels are present or not (31). Subsequently, a “neuron-to-model matched” (NMM) approach was used to create new OLM cell models in which there was a tight integration of experimental data with the multi-compartment model building, so as to determine whether dendritic h-channels are in fact present or absent (27) . These new OLM models created using this NMM approach strongly suggested that h-channels must be present on OLM cell dendrites.…”

Section: Introductionmentioning

confidence: 99%

“…In this study, we use computational modelling and theoretical analyses to examine how I-S3 cells manifest control over OLM cells so as to decipher how these specialized cell types contribute to function. In the strategy implemented in this work, we use the new OLM cell models (27) with synaptic inputs from I-S3 cells as well as other inputs (33), and perform simulations with these models under in vitro and in vivo -like contexts (see Fig 1 illustration), as motivated by experimental data specific to OLM and I-S3 cells. Our explorations in the in vitro context are based on observations from Tyan et al (15) which showed that I-S3 cells could preferentially control the timing of OLM cell spiking at 5 and 10 Hz (theta frequencies) but not at non-theta frequencies.…”

Section: Introductionmentioning

confidence: 99%

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Deciphering how interneuron specific 3 cells control oriens lacunosum-moleculare cells to contribute to circuit function

Guet-McCreight

Skinner

2020

Preprint

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The wide diversity of inhibitory cells across the brain makes them fit to contribute to network dynamics in specialized fashions. However, the contributions of a particular inhibitory cell type in a behaving animal is challenging to decipher as one needs to both record cellular activities and identify the cell type being recorded. Thus, using computational modeling to explore cell-specific contributions so as to predict and hypothesize functional contributions is desirable. Here we examine potential contributions of interneuron-specific 3 (I-S3) cells - a type of inhibitory interneuron found in CA1 hippocampus that only targets other inhibitory interneurons - during simulated theta rhythms. We use previously developed multi-compartment models of oriens lacunosum-moleculare (OLM) cells, the main target of I-S3 cells, and explore how I-S3 cell inputs during in vitro and in vivo scenarios contribute to theta. We find that I-S3 cells suppress OLM cell spiking, rather than engender its spiking via post-inhibitory rebound mechanisms. To elicit recruitment similar to experiment, the inclusion of disinhibited pyramidal cell inputs is necessary, suggesting that I-S3 cell firing can broaden the window for disinhibiting pyramidal cells. Using in vivo virtual networks, we show that I-S3 cells can contribute to a sharpening of OLM cell recruitment at theta frequencies. Further, a shifting of the timing of I-S3 cell spiking due to external modulation can shift the timing of the OLM cell firing and thus disinhibitory windows. We thus propose a specialized contribution of I-S3 cells to create temporally precise coordination of modulation pathways.Significance StatementHow information is processed across different brain structures is an important question that relates to the different functions that the brain performs. In this work we use computational models that focus on a particular inhibitory cell type that only inhibits other inhibitory cell types – the I-S3 cell in the hippocampus. We show that this cell type is able to broaden the window for disinhibition of excitatory cells. We further illustrate that this broadening presents itself as a mechanism for input pathway switching and modulation over the timing of inhibitory cell spiking. Overall, this work contributes to our knowledge of how coordination between sensory and memory consolidation information is attained in a brain area that is involved in memory formation.

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Adaptive unscented Kalman filter for neuronal state and parameter estimation

et al. 2023

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Data assimilation techniques for state and parameter estimation are frequently applied in the context of computational neuroscience. In this work, we show how an adaptive variant of the unscented Kalman filter (UKF) performs on the tracking of a conductance-based neuron model. Unlike standard recursive filter implementations, the robust adaptive unscented Kalman filter (RAUKF) jointly estimates the states and parameters of the neuronal model while adjusting noise covariance matrices online based on innovation and residual information. We benchmark the adaptive filter's performance against existing nonlinear Kalman filters and explore the sensitivity of the filter parameters to the system being modelled. To evaluate the robustness of the proposed solution, we simulate practical settings that challenge tracking performance, such as a model mismatch and measurement faults. Compared to standard variants of the Kalman filter the adaptive variant implemented here is more accurate and robust to faults.

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Integration of Within-Cell Experimental Data With Multi-Compartmental Modeling Predicts H-Channel Densities and Distributions in Hippocampal OLM Cells

Cited by 11 publications

References 93 publications

Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression

Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression

Deciphering how interneuron specific 3 cells control oriens lacunosum-moleculare cells to contribute to circuit function

Adaptive unscented Kalman filter for neuronal state and parameter estimation

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