Circuit mechanisms for the chemical modulation of cortex-wide network interactions and behavioral variability

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Circuit mechanisms for the chemical modulation of cortex-wide network interactions and behavioral variability. / Pfeffer, Thomas; Ponce-Alvarez, Adrian; Tsetsos, Konstantinos; Meindertsma, Thomas; Gahnström, Christoffer Julius; van den Brink, Ruud Lucas; Nolte, Guido; Engel, Andreas Karl; Deco, Gustavo; Donner, Tobias Hinrich.

in: SCI ADV, Jahrgang 7, Nr. 29, eabf5620, 07.2021.

Publikationen: SCORING: Beitrag in Fachzeitschrift/ZeitungSCORING: ZeitschriftenaufsatzForschungBegutachtung

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@article{e189c13c5a5d4fd381ed0dcf42189a7a,
title = "Circuit mechanisms for the chemical modulation of cortex-wide network interactions and behavioral variability",
abstract = "Influential theories postulate distinct roles of catecholamines and acetylcholine in cognition and behavior. However, previous physiological work reported similar effects of these neuromodulators on the response properties (specifically, the gain) of individual cortical neurons. Here, we show a double dissociation between the effects of catecholamines and acetylcholine at the level of large-scale interactions between cortical areas in humans. A pharmacological boost of catecholamine levels increased cortex-wide interactions during a visual task, but not rest. An acetylcholine boost decreased interactions during rest, but not task. Cortical circuit modeling explained this dissociation by differential changes in two circuit properties: the local excitation-inhibition balance (more strongly increased by catecholamines) and intracortical transmission (more strongly reduced by acetylcholine). The inferred catecholaminergic mechanism also predicted noisier decision-making, which we confirmed for both perceptual and value-based choice behavior. Our work highlights specific circuit mechanisms for shaping cortical network interactions and behavioral variability by key neuromodulatory systems.",
author = "Thomas Pfeffer and Adrian Ponce-Alvarez and Konstantinos Tsetsos and Thomas Meindertsma and Gahnstr{\"o}m, {Christoffer Julius} and {van den Brink}, {Ruud Lucas} and Guido Nolte and Engel, {Andreas Karl} and Gustavo Deco and Donner, {Tobias Hinrich}",
note = "Copyright {\textcopyright} 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).",
year = "2021",
month = jul,
doi = "10.1126/sciadv.abf5620",
language = "English",
volume = "7",
journal = "SCI ADV",
issn = "2375-2548",
publisher = "American Association for the Advancement of Science",
number = "29",

}

RIS

TY - JOUR

T1 - Circuit mechanisms for the chemical modulation of cortex-wide network interactions and behavioral variability

AU - Pfeffer, Thomas

AU - Ponce-Alvarez, Adrian

AU - Tsetsos, Konstantinos

AU - Meindertsma, Thomas

AU - Gahnström, Christoffer Julius

AU - van den Brink, Ruud Lucas

AU - Nolte, Guido

AU - Engel, Andreas Karl

AU - Deco, Gustavo

AU - Donner, Tobias Hinrich

N1 - Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

PY - 2021/7

Y1 - 2021/7

N2 - Influential theories postulate distinct roles of catecholamines and acetylcholine in cognition and behavior. However, previous physiological work reported similar effects of these neuromodulators on the response properties (specifically, the gain) of individual cortical neurons. Here, we show a double dissociation between the effects of catecholamines and acetylcholine at the level of large-scale interactions between cortical areas in humans. A pharmacological boost of catecholamine levels increased cortex-wide interactions during a visual task, but not rest. An acetylcholine boost decreased interactions during rest, but not task. Cortical circuit modeling explained this dissociation by differential changes in two circuit properties: the local excitation-inhibition balance (more strongly increased by catecholamines) and intracortical transmission (more strongly reduced by acetylcholine). The inferred catecholaminergic mechanism also predicted noisier decision-making, which we confirmed for both perceptual and value-based choice behavior. Our work highlights specific circuit mechanisms for shaping cortical network interactions and behavioral variability by key neuromodulatory systems.

AB - Influential theories postulate distinct roles of catecholamines and acetylcholine in cognition and behavior. However, previous physiological work reported similar effects of these neuromodulators on the response properties (specifically, the gain) of individual cortical neurons. Here, we show a double dissociation between the effects of catecholamines and acetylcholine at the level of large-scale interactions between cortical areas in humans. A pharmacological boost of catecholamine levels increased cortex-wide interactions during a visual task, but not rest. An acetylcholine boost decreased interactions during rest, but not task. Cortical circuit modeling explained this dissociation by differential changes in two circuit properties: the local excitation-inhibition balance (more strongly increased by catecholamines) and intracortical transmission (more strongly reduced by acetylcholine). The inferred catecholaminergic mechanism also predicted noisier decision-making, which we confirmed for both perceptual and value-based choice behavior. Our work highlights specific circuit mechanisms for shaping cortical network interactions and behavioral variability by key neuromodulatory systems.

U2 - 10.1126/sciadv.abf5620

DO - 10.1126/sciadv.abf5620

M3 - SCORING: Journal article

C2 - 34272245

VL - 7

JO - SCI ADV

JF - SCI ADV

SN - 2375-2548

IS - 29

M1 - eabf5620

ER -