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Are single-peaked tuning curves tuned for speed rather than accuracy?

According to the efficient coding hypothesis, sensory neurons are adapted to provide maximal information about the environment, given some biophysical constraints. In early visual areas, stimulus-induced modulations of neural activity (or tunings) are predominantly single-peaked. However, periodic t...

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Autores principales: Lenninger, Movitz, Skoglund, Mikael, Herman, Pawel Andrzej, Kumar, Arvind
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10259479/
https://www.ncbi.nlm.nih.gov/pubmed/37191292
http://dx.doi.org/10.7554/eLife.84531
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author Lenninger, Movitz
Skoglund, Mikael
Herman, Pawel Andrzej
Kumar, Arvind
author_facet Lenninger, Movitz
Skoglund, Mikael
Herman, Pawel Andrzej
Kumar, Arvind
author_sort Lenninger, Movitz
collection PubMed
description According to the efficient coding hypothesis, sensory neurons are adapted to provide maximal information about the environment, given some biophysical constraints. In early visual areas, stimulus-induced modulations of neural activity (or tunings) are predominantly single-peaked. However, periodic tuning, as exhibited by grid cells, has been linked to a significant increase in decoding performance. Does this imply that the tuning curves in early visual areas are sub-optimal? We argue that the time scale at which neurons encode information is imperative to understand the advantages of single-peaked and periodic tuning curves, respectively. Here, we show that the possibility of catastrophic (large) errors creates a trade-off between decoding time and decoding ability. We investigate how decoding time and stimulus dimensionality affect the optimal shape of tuning curves for removing catastrophic errors. In particular, we focus on the spatial periods of the tuning curves for a class of circular tuning curves. We show an overall trend for minimal decoding time to increase with increasing Fisher information, implying a trade-off between accuracy and speed. This trade-off is reinforced whenever the stimulus dimensionality is high, or there is ongoing activity. Thus, given constraints on processing speed, we present normative arguments for the existence of the single-peaked tuning organization observed in early visual areas.
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spelling pubmed-102594792023-06-13 Are single-peaked tuning curves tuned for speed rather than accuracy? Lenninger, Movitz Skoglund, Mikael Herman, Pawel Andrzej Kumar, Arvind eLife Neuroscience According to the efficient coding hypothesis, sensory neurons are adapted to provide maximal information about the environment, given some biophysical constraints. In early visual areas, stimulus-induced modulations of neural activity (or tunings) are predominantly single-peaked. However, periodic tuning, as exhibited by grid cells, has been linked to a significant increase in decoding performance. Does this imply that the tuning curves in early visual areas are sub-optimal? We argue that the time scale at which neurons encode information is imperative to understand the advantages of single-peaked and periodic tuning curves, respectively. Here, we show that the possibility of catastrophic (large) errors creates a trade-off between decoding time and decoding ability. We investigate how decoding time and stimulus dimensionality affect the optimal shape of tuning curves for removing catastrophic errors. In particular, we focus on the spatial periods of the tuning curves for a class of circular tuning curves. We show an overall trend for minimal decoding time to increase with increasing Fisher information, implying a trade-off between accuracy and speed. This trade-off is reinforced whenever the stimulus dimensionality is high, or there is ongoing activity. Thus, given constraints on processing speed, we present normative arguments for the existence of the single-peaked tuning organization observed in early visual areas. eLife Sciences Publications, Ltd 2023-05-16 /pmc/articles/PMC10259479/ /pubmed/37191292 http://dx.doi.org/10.7554/eLife.84531 Text en © 2023, Lenninger et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Lenninger, Movitz
Skoglund, Mikael
Herman, Pawel Andrzej
Kumar, Arvind
Are single-peaked tuning curves tuned for speed rather than accuracy?
title Are single-peaked tuning curves tuned for speed rather than accuracy?
title_full Are single-peaked tuning curves tuned for speed rather than accuracy?
title_fullStr Are single-peaked tuning curves tuned for speed rather than accuracy?
title_full_unstemmed Are single-peaked tuning curves tuned for speed rather than accuracy?
title_short Are single-peaked tuning curves tuned for speed rather than accuracy?
title_sort are single-peaked tuning curves tuned for speed rather than accuracy?
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10259479/
https://www.ncbi.nlm.nih.gov/pubmed/37191292
http://dx.doi.org/10.7554/eLife.84531
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