Neocortex saves energy by reducing coding precision during food scarcity
Zahid Padamsey, Danai Katsanevaki, Nathalie Dupuy, Nathalie L Rochefort
Abstract
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.
Keywords: calorie restriction; hunger and satiety; in vivo ATP imaging; in vivo calcium imaging; in vivo electrophysiology; leptin; mouse primary visual cortex; orientation tuning; spike rate homeostasis; trial-to-trial variability.
Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.
Conflict of interest statement
Declaration of interests The authors declare no competing interests
https://www.cell.com/neuron/fulltext/S0896-6273(21)00839-4?_returnURL=https://linkinghub.elsevier.com/retrieve/pii/S0896627321008394?showall=true#
Note:
This study is in mice - but might be of interest if calorie restriction is a proxy for otherwise reduced energy availability for the mammalian brain.
Zahid Padamsey, Danai Katsanevaki, Nathalie Dupuy, Nathalie L Rochefort
Abstract
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.
Keywords: calorie restriction; hunger and satiety; in vivo ATP imaging; in vivo calcium imaging; in vivo electrophysiology; leptin; mouse primary visual cortex; orientation tuning; spike rate homeostasis; trial-to-trial variability.
Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.
Conflict of interest statement
Declaration of interests The authors declare no competing interests
https://www.cell.com/neuron/fulltext/S0896-6273(21)00839-4?_returnURL=https://linkinghub.elsevier.com/retrieve/pii/S0896627321008394?showall=true#
Note:
This study is in mice - but might be of interest if calorie restriction is a proxy for otherwise reduced energy availability for the mammalian brain.
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