Dataset Information

Axonal Anatomy Optimizes Spatial Encoding in the Rat Entorhinal-Dentate System: A Computational Study.

ABSTRACT: OBJECTIVE:The network architecture connecting neural regions is defined by the organization and anatomical properties of the projecting axons, but its contributions to neural encoding and system function are difficult to study experimentally. METHODS:Using a large-scale, spiking neuronal network model of rat dentate gyrus, the role of the anatomy of the entorhinal-dentate axonal projection was evaluated in the context of spatial encoding by incorporating grid cell activity to provide physiological, spatially-correlated input. The dorso-ventral extents of the entorhinal axon terminal fields were varied to generate different feedforward architectures, and the resulting spatial representations and spatial information scores of the network were evaluated. Position was decoded from the population activity using a point process filter to investigate the contributions of network architecture on spatial encoding. RESULTS:The model predicted the emergence of anatomical gradients within the dentate gyrus for place field size and spatial information along its dorso-ventral axis, which were dependent on the extents of the entorhinal axon terminal fields. The decoding results revealed an optimal performance at an axon terminal field extent of 2 mm that lies within the biological range. CONCLUSION:The axonal anatomy mediates a tradeoff between encoding multiple place field sizes or achieving a high spatial information score, and the combination of both properties is necessary to maximize spatial encoding by a network. SIGNIFICANCE:In total, this paper establishes a mechanistic neuronal network model that, in concert with information-theoretic and statistical methods, can be used to investigate how lower level properties contribute to higher level function.

SUBMITTER: Yu GJ

PROVIDER: S-EPMC6642851 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Axonal Anatomy Optimizes Spatial Encoding in the Rat Entorhinal-Dentate System: A Computational Study.

Yu Gene J GJ Bouteiller Jean-Marie C JC Song Dong D Berger Theodore W TW

IEEE transactions on bio-medical engineering 20190121 10

<h4>Objective</h4>The network architecture connecting neural regions is defined by the organization and anatomical properties of the projecting axons, but its contributions to neural encoding and system function are difficult to study experimentally.<h4>Methods</h4>Using a large-scale, spiking neuronal network model of rat dentate gyrus, the role of the anatomy of the entorhinal-dentate axonal projection was evaluated in the context of spatial encoding by incorporating grid cell activity to prov ...[more]

PMID: 30676938

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Project description:OBJECTIVE:Functions ascribed to the hippocampal sub-regions for encoding episodic memories include the separation of activity patterns propagated from the entorhinal cortex (EC) into the dentate gyrus (DG) and pattern completion in CA3 region. Since a direct assessment of these functions is lacking at the level of specific axonal inputs, our goal is to directly measure the separation and completion of distinct axonal inputs in engineered pairs of hippocampal sub-regional circuits. APPROACH:We co-cultured EC-DG, DG-CA3, CA3-CA1 or CA1-EC neurons in a two-chamber PDMS device over a micro-electrode array (MEA60), inter-connected via distinct axons that grow through the micro-tunnels between the compartments. Taking advantage of the axonal accessibility, we quantified pattern separation and completion of the evoked activity transmitted through the tunnels from source into target well. Since pattern separation can be inferred when inputs are more correlated than outputs, we first compared the correlations among axonal inputs with those of target somata outputs. We then compared, in an analog approach, the distributions of correlation distances between rate patterns of the axonal inputs inside the tunnels with those of the somata outputs evoked in the target well. Finally, in a digital approach, we measured the spatial population distances between binary patterns of the same axonal inputs and somata outputs. MAIN RESULTS:We found the strongest separation of the propagated axonal inputs when EC was axonally connected to DG, with a decline in separation to CA3 and to CA1 for both rate and digital approaches. Furthermore, the digital approach showed stronger pattern completion in CA3, then CA1 and EC. SIGNIFICANCE:To the best of our knowledge, these are the first direct measures of pattern separation and completion for axonal transmission to the somata target outputs at the rate and digital population levels in each of four stages of the EC-DG-CA3-CA1 circuit.

Dataset Information

Axonal Anatomy Optimizes Spatial Encoding in the Rat Entorhinal-Dentate System: A Computational Study.

Publications

Axonal Anatomy Optimizes Spatial Encoding in the Rat Entorhinal-Dentate System: A Computational Study.

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