Spatial information transfer in hippocampal place cells depends on trial-to-trial variability, symmetry of place-field firing, and biophysical heterogeneities.
Degeneracy
Ion channels
Mutual information
Stimulus specific information
Tuning curve
Journal
Neural networks : the official journal of the International Neural Network Society
ISSN: 1879-2782
Titre abrégé: Neural Netw
Pays: United States
ID NLM: 8805018
Informations de publication
Date de publication:
Oct 2021
Oct 2021
Historique:
received:
18
09
2020
revised:
25
03
2021
accepted:
21
07
2021
pubmed:
17
8
2021
medline:
25
11
2021
entrez:
16
8
2021
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 34399375
pii: S0893-6080(21)00297-5
doi: 10.1016/j.neunet.2021.07.026
pmc: PMC7611579
mid: EMS133047
pii:
doi:
Substances chimiques
Receptors, N-Methyl-D-Aspartate
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
636-660Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : DBT-Wellcome Trust India Alliance
ID : IA/S/16/2/502727
Pays : India
Informations de copyright
Copyright © 2021 The Author(s). Published by Elsevier Ltd.. All rights reserved.
Déclaration de conflit d'intérêts
Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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