Cargando…

Neocortex saves energy by reducing coding precision during food scarcity

Information processing is energetically expensive. In the mammalian brain, it is unclear how information coding and energy use are regulated during food scarcity. Using whole-cell recordings and two-photon imaging in layer 2/3 mouse visual cortex, we found that food restriction reduced AMPA receptor...

Descripción completa

Detalles Bibliográficos
Autores principales: Padamsey, Zahid, Katsanevaki, Danai, Dupuy, Nathalie, Rochefort, Nathalie L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8788933/
https://www.ncbi.nlm.nih.gov/pubmed/34741806
http://dx.doi.org/10.1016/j.neuron.2021.10.024
_version_ 1784639656300642304
author Padamsey, Zahid
Katsanevaki, Danai
Dupuy, Nathalie
Rochefort, Nathalie L.
author_facet Padamsey, Zahid
Katsanevaki, Danai
Dupuy, Nathalie
Rochefort, Nathalie L.
author_sort Padamsey, Zahid
collection PubMed
description Information processing is energetically expensive. In the mammalian brain, it is unclear how information coding and energy use are regulated during food scarcity. Using whole-cell recordings and two-photon imaging in layer 2/3 mouse visual cortex, we found that food restriction reduced AMPA receptor conductance, reducing synaptic ATP use by 29%. Neuronal excitability was nonetheless preserved by a compensatory increase in input resistance and a depolarized resting potential. Consequently, neurons spiked at similar rates as controls but spent less ATP on underlying excitatory currents. This energy-saving strategy had a cost because it amplified the variability of visually-evoked subthreshold responses, leading to a 32% broadening of orientation tuning and impaired fine visual discrimination. This reduction in coding precision was associated with reduced levels of the fat mass-regulated hormone leptin and was restored by exogenous leptin supplementation. Our findings reveal that metabolic state dynamically regulates the energy spent on coding precision in neocortex.
format Online
Article
Text
id pubmed-8788933
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Cell Press
record_format MEDLINE/PubMed
spelling pubmed-87889332022-02-01 Neocortex saves energy by reducing coding precision during food scarcity Padamsey, Zahid Katsanevaki, Danai Dupuy, Nathalie Rochefort, Nathalie L. Neuron Article Information processing is energetically expensive. In the mammalian brain, it is unclear how information coding and energy use are regulated during food scarcity. Using whole-cell recordings and two-photon imaging in layer 2/3 mouse visual cortex, we found that food restriction reduced AMPA receptor conductance, reducing synaptic ATP use by 29%. Neuronal excitability was nonetheless preserved by a compensatory increase in input resistance and a depolarized resting potential. Consequently, neurons spiked at similar rates as controls but spent less ATP on underlying excitatory currents. This energy-saving strategy had a cost because it amplified the variability of visually-evoked subthreshold responses, leading to a 32% broadening of orientation tuning and impaired fine visual discrimination. This reduction in coding precision was associated with reduced levels of the fat mass-regulated hormone leptin and was restored by exogenous leptin supplementation. Our findings reveal that metabolic state dynamically regulates the energy spent on coding precision in neocortex. Cell Press 2022-01-19 /pmc/articles/PMC8788933/ /pubmed/34741806 http://dx.doi.org/10.1016/j.neuron.2021.10.024 Text en © 2021 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Padamsey, Zahid
Katsanevaki, Danai
Dupuy, Nathalie
Rochefort, Nathalie L.
Neocortex saves energy by reducing coding precision during food scarcity
title Neocortex saves energy by reducing coding precision during food scarcity
title_full Neocortex saves energy by reducing coding precision during food scarcity
title_fullStr Neocortex saves energy by reducing coding precision during food scarcity
title_full_unstemmed Neocortex saves energy by reducing coding precision during food scarcity
title_short Neocortex saves energy by reducing coding precision during food scarcity
title_sort neocortex saves energy by reducing coding precision during food scarcity
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8788933/
https://www.ncbi.nlm.nih.gov/pubmed/34741806
http://dx.doi.org/10.1016/j.neuron.2021.10.024
work_keys_str_mv AT padamseyzahid neocortexsavesenergybyreducingcodingprecisionduringfoodscarcity
AT katsanevakidanai neocortexsavesenergybyreducingcodingprecisionduringfoodscarcity
AT dupuynathalie neocortexsavesenergybyreducingcodingprecisionduringfoodscarcity
AT rochefortnathaliel neocortexsavesenergybyreducingcodingprecisionduringfoodscarcity