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Spatial information transfer in hippocampal place cells depends on trial-to-trial variability, symmetry of place-field firing, and biophysical heterogeneities

Roy, A and Narayanan, R (2021) Spatial information transfer in hippocampal place cells depends on trial-to-trial variability, symmetry of place-field firing, and biophysical heterogeneities. In: Neural Networks, 142 . pp. 636-660.

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Official URL: https://doi.org/10.1016/j.neunet.2021.07.026

Abstract

The relationship between the feature-tuning curve and information transfer profile of individual neurons provides vital insights about neural encoding. However, the relationship between the spatial tuning curve and spatial information transfer of hippocampal place cells remains unexplored. Here, employing a stochastic search procedure spanning thousands of models, we arrived at 127 conductance-based place-cell models that exhibited signature electrophysiological characteristics and sharp spatial tuning, with parametric values that exhibited neither clustering nor strong pairwise correlations. We introduced trial-to-trial variability in responses and computed model tuning curves and information transfer profiles, using stimulus-specific (SSI) and mutual (MI) information metrics, across locations within the place field. We found spatial information transfer to be heterogeneous across models, but to reduce consistently with increasing levels of variability. Importantly, whereas reliable low-variability responses implied that maximal information transfer occurred at high-slope regions of the tuning curve, increase in variability resulted in maximal transfer occurring at the peak-firing location in a subset of models. Moreover, experience-dependent asymmetry in place-field firing introduced asymmetries in the information transfer computed through MI, but not SSI, and the impact of activity-dependent variability on information transfer was minimal compared to activity-independent variability. We unveiled ion-channel degeneracy in the regulation of spatial information transfer, and demonstrated critical roles for N-methyl-D-aspartate receptors, transient potassium and dendritic sodium channels in regulating information transfer. Our results demonstrate that trial-to-trial variability, tuning-curve shape and biological heterogeneities critically regulate the relationship between the spatial tuning curve and spatial information transfer in hippocampal place cells. © 2021 The Author(s)

Item Type: Journal Article
Publication: Neural Networks
Publisher: Elsevier Ltd
Additional Information: The copyright for this article belongs to Authors
Keywords: Cytology; Electrophysiology; Neurons; Stochastic models; Stochastic systems, Degeneracy; Hippocampal place cells; Information transfers; Ion channel; Mutual informations; Neural encoding; Spatial informations; Stimulus specific information; Trial-to-trial variabilities; Tuning curve, Cells
Department/Centre: Division of Biological Sciences > Molecular Biophysics Unit
UG Programme
Date Deposited: 21 Sep 2021 09:31
Last Modified: 21 Sep 2021 09:31
URI: http://eprints.iisc.ac.in/id/eprint/69752

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