Receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays.

Studies on population coding implicitly assume that spikes from the presynaptic cells arrive simultaneously at the integrating neuron. In natural neuronal populations, this is usually not the case-neuronal signaling takes time and populations cover a certain space. The spread of spike arrival times...

Full description

Bibliographic Details
Main Authors: Tim C Hladnik, Jan Grewe
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-08-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1010871
_version_ 1827104341054455808
author Tim C Hladnik
Jan Grewe
author_facet Tim C Hladnik
Jan Grewe
author_sort Tim C Hladnik
collection DOAJ
description Studies on population coding implicitly assume that spikes from the presynaptic cells arrive simultaneously at the integrating neuron. In natural neuronal populations, this is usually not the case-neuronal signaling takes time and populations cover a certain space. The spread of spike arrival times depends on population size, cell density and axonal conduction velocity. Here we analyze the consequences of population size and axonal conduction delays on the stimulus encoding performance in the electrosensory system of the electric fish Apteronotus leptorhynchus. We experimentally locate p-type electroreceptor afferents along the rostro-caudal body axis and relate locations to neurophysiological response properties. In an information-theoretical approach we analyze the coding performance in homogeneous and heterogeneous populations. As expected, the amount of information increases with population size and, on average, heterogeneous populations encode better than the average same-size homogeneous population, if conduction delays are compensated for. The spread of neuronal conduction delays within a receptive field strongly degrades encoding of high-frequency stimulus components. Receptive field sizes typically found in the electrosensory lateral line lobe of A. leptorhynchus appear to be a good compromise between the spread of conduction delays and encoding performance. The limitations imposed by finite axonal conduction velocity are relevant for any converging network as is shown by model populations of LIF neurons. The bandwidth of natural stimuli and the maximum meaningful population sizes are constrained by conduction delays and may thus impact the optimal design of nervous systems.
first_indexed 2024-03-11T21:53:27Z
format Article
id doaj.art-2e5a449b4ff946e4ba290c234449ea7e
institution Directory Open Access Journal
issn 1553-734X
1553-7358
language English
last_indexed 2025-03-20T09:21:23Z
publishDate 2023-08-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS Computational Biology
spelling doaj.art-2e5a449b4ff946e4ba290c234449ea7e2024-09-26T05:31:23ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582023-08-01198e101087110.1371/journal.pcbi.1010871Receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays.Tim C HladnikJan GreweStudies on population coding implicitly assume that spikes from the presynaptic cells arrive simultaneously at the integrating neuron. In natural neuronal populations, this is usually not the case-neuronal signaling takes time and populations cover a certain space. The spread of spike arrival times depends on population size, cell density and axonal conduction velocity. Here we analyze the consequences of population size and axonal conduction delays on the stimulus encoding performance in the electrosensory system of the electric fish Apteronotus leptorhynchus. We experimentally locate p-type electroreceptor afferents along the rostro-caudal body axis and relate locations to neurophysiological response properties. In an information-theoretical approach we analyze the coding performance in homogeneous and heterogeneous populations. As expected, the amount of information increases with population size and, on average, heterogeneous populations encode better than the average same-size homogeneous population, if conduction delays are compensated for. The spread of neuronal conduction delays within a receptive field strongly degrades encoding of high-frequency stimulus components. Receptive field sizes typically found in the electrosensory lateral line lobe of A. leptorhynchus appear to be a good compromise between the spread of conduction delays and encoding performance. The limitations imposed by finite axonal conduction velocity are relevant for any converging network as is shown by model populations of LIF neurons. The bandwidth of natural stimuli and the maximum meaningful population sizes are constrained by conduction delays and may thus impact the optimal design of nervous systems.https://doi.org/10.1371/journal.pcbi.1010871
spellingShingle Tim C Hladnik
Jan Grewe
Receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays.
PLoS Computational Biology
title Receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays.
title_full Receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays.
title_fullStr Receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays.
title_full_unstemmed Receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays.
title_short Receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays.
title_sort receptive field sizes and neuronal encoding bandwidth are constrained by axonal conduction delays
url https://doi.org/10.1371/journal.pcbi.1010871
work_keys_str_mv AT timchladnik receptivefieldsizesandneuronalencodingbandwidthareconstrainedbyaxonalconductiondelays
AT jangrewe receptivefieldsizesandneuronalencodingbandwidthareconstrainedbyaxonalconductiondelays