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Microstructural and neurochemical plasticity mechanisms interact to enhance human perceptual decision-making.

Published version
Peer-reviewed

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Authors

Ziminski, Joseph J 
Frangou, Polytimi 
Karlaftis, Vasilis M 
Emir, Uzay 

Abstract

Experience and training are known to boost our skills and mold the brain's organization and function. Yet, structural plasticity and functional neurotransmission are typically studied at different scales (large-scale networks, local circuits), limiting our understanding of the adaptive interactions that support learning of complex cognitive skills in the adult brain. Here, we employ multimodal brain imaging to investigate the link between microstructural (myelination) and neurochemical (GABAergic) plasticity for decision-making. We test (in males, due to potential confounding menstrual cycle effects on GABA measurements in females) for changes in MRI-measured myelin, GABA, and functional connectivity before versus after training on a perceptual decision task that involves identifying targets in clutter. We demonstrate that training alters subcortical (pulvinar, hippocampus) myelination and its functional connectivity to visual cortex and relates to decreased visual cortex GABAergic inhibition. Modeling interactions between MRI measures of myelin, GABA, and functional connectivity indicates that pulvinar myelin plasticity interacts-through thalamocortical connectivity-with GABAergic inhibition in visual cortex to support learning. Our findings propose a dynamic interplay of adaptive microstructural and neurochemical plasticity in subcortico-cortical circuits that supports learning for optimized decision-making in the adult human brain.

Description

Acknowledgements: We would like to thank the MR physics and radiographer teams at the Cambridge Wolfson Brain Imaging Centre, and Lilia Kukovska for their support and help with data collection. We would also like to thank Martina Callaghan, Nickolas Weiskopf, and the Wellcome Centre for Human Neuroimaging for providing the MPM sequences, and Guy Williams and Steve Sawiak for their expert assistance in MR-sequence testing. We would like to thank Thora Karadottir, Sonja Hofer, Jasper Poort, and Martina Callaghan for helpful comments and suggestions.

Keywords

Adult, Male, Female, Humans, Learning, Brain, Magnetic Resonance Imaging, Brain Mapping, gamma-Aminobutyric Acid, Neuronal Plasticity

Journal Title

PLoS Biol

Conference Name

Journal ISSN

1544-9173
1545-7885

Volume Title

Publisher

Public Library of Science (PLoS)
Sponsorship
Wellcome Trust (205067/Z/16/Z)
Biotechnology and Biological Sciences Research Council (BB/P021255/1)
Wellcome Trust (223131/Z/21/Z)
Wellcome Trust (221633/Z/20/Z)
This work was supported by grants to ZK from the Wellcome Trust [grant number 205067/Z/16/Z, 221633/Z/20/Z], the Biotechnology and Biological Sciences Research Council [grant numbers H012508, BB/P021255/1].
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