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Modelling unitary fields and the single-neuron contribution to local field potentials in the hippocampus.

ABSTRACT: KEY POINTS:We simulate the unitary local field potential (uLFP) generated in the hippocampus CA3, using morphologically detailed models. The model suggests that cancelling effects between apical and basal dendritic synapses explain the low amplitude of excitatory uLFPs. Inhibitory synapses around the soma do not cancel and could explain the high-amplitude inhibitory uLFPs. These results suggest that somatic inhibition constitutes a strong component of LFPs, which may explain a number of experimental observations. ABSTRACT:Synaptic currents represent a major contribution to the local field potential (LFP) in brain tissue, but the respective contribution of excitatory and inhibitory synapses is not known. Here, we provide estimates of this contribution by using computational models of hippocampal pyramidal neurons, constrained by in vitro recordings. We focus on the unitary LFP (uLFP) generated by single neurons in the CA3 region of the hippocampus. We first reproduce experimental results for hippocampal basket cells, and in particular how inhibitory uLFP are distributed within hippocampal layers. Next, we calculate the uLFP generated by pyramidal neurons, using morphologically reconstructed CA3 pyramidal cells. The model shows that the excitatory uLFP is of small amplitude, smaller than inhibitory uLFPs. Indeed, when the two are simulated together, inhibitory uLFPs mask excitatory uLFPs, which might create the illusion that the inhibitory field is generated by pyramidal cells. These results provide an explanation for the observation that excitatory and inhibitory uLFPs are of the same polarity, in vivo and in vitro. These results suggest that somatic inhibitory currents are large contributors to the LFP, which is important information for interpreting this signal. Finally, the results of our model might form the basis of a simple method to compute the LFP, which could be applied to point neurons for each cell type, thus providing a simple biologically grounded method for calculating LFPs from neural networks. In conclusion, computational models constrained by in vitro recordings suggest that: (1) Excitatory uLFPs are of smaller amplitude than inhibitory uLFPs. (2) Inhibitory uLFPs form the major contribution to LFPs. (3) uLFPs can be used as a simple model to generate LFPs from spiking networks.

SUBMITTER: Telenczuk M

PROVIDER: S-EPMC7540286 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Modelling unitary fields and the single-neuron contribution to local field potentials in the hippocampus.

Teleńczuk Maria M Teleńczuk Bartosz B Destexhe Alain A

The Journal of physiology 20200709 18

<h4>Key points</h4>We simulate the unitary local field potential (uLFP) generated in the hippocampus CA3, using morphologically detailed models. The model suggests that cancelling effects between apical and basal dendritic synapses explain the low amplitude of excitatory uLFPs. Inhibitory synapses around the soma do not cancel and could explain the high-amplitude inhibitory uLFPs. These results suggest that somatic inhibition constitutes a strong component of LFPs, which may explain a number of ...[more]

PMID: 32598027

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Project description:Significant progress has been made toward model-based prediction of neral tissue activation in response to extracellular electrical stimulation, but challenges remain in the accurate and efficient estimation of distributed local field potentials (LFP). Analytical methods of estimating electric fields are a first-order approximation that may be suitable for model validation, but they are computationally expensive and cannot accurately capture boundary conditions in heterogeneous tissue. While there are many appropriate numerical methods of solving electric fields in neural tissue models, there isn't an established standard for mesh geometry nor a well-known rule for handling any mismatch in spatial resolution. Moreover, the challenge of misalignment between current sources and mesh nodes in a finite-element or resistor-network method volume conduction model needs to be further investigated. Therefore, using a previously published and validated multi-scale model of the hippocampus, the authors have formulated an algorithm for LFP estimation, and by extension, bidirectional communication between discretized and numerically solved volume conduction models and biologically detailed neural circuit models constructed in NEURON. Development of this algorithm required that we assess meshes of (i) unstructured tetrahedral and grid-based hexahedral geometries as well as (ii) differing approaches for managing the spatial misalignment of current sources and mesh nodes. The resulting algorithm is validated through the comparison of Admittance Method predicted evoked potentials with analytically estimated LFPs. Establishing this method is a critical step toward closed-loop integration of volume conductor and NEURON models that could lead to substantial improvement of the predictive power of multi-scale stimulation models of cortical tissue. These models may be used to deepen our understanding of hippocampal pathologies and the identification of efficacious electroceutical treatments.

Dataset Information

Modelling unitary fields and the single-neuron contribution to local field potentials in the hippocampus.

Publications

Modelling unitary fields and the single-neuron contribution to local field potentials in the hippocampus.

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