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Trust your gut: vagal nerve stimulation in humans improves reinforcement learning

Whereas the effect of vagal nerve stimulation on emotional states is well established, its effect on cognitive functions is still unclear. Recent rodent studies show that vagal activation enhances reinforcement learning and neuronal dopamine release. The influence of vagal nerve stimulation on reinf...

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Autores principales: Weber, Immo, Niehaus, Hauke, Krause, Kristina, Molitor, Lena, Peper, Martin, Schmidt, Laura, Hakel, Lukas, Timmermann, Lars, Menzler, Katja, Knake, Susanne, Oehrn, Carina R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8066886/
https://www.ncbi.nlm.nih.gov/pubmed/33928247
http://dx.doi.org/10.1093/braincomms/fcab039
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author Weber, Immo
Niehaus, Hauke
Krause, Kristina
Molitor, Lena
Peper, Martin
Schmidt, Laura
Hakel, Lukas
Timmermann, Lars
Menzler, Katja
Knake, Susanne
Oehrn, Carina R
author_facet Weber, Immo
Niehaus, Hauke
Krause, Kristina
Molitor, Lena
Peper, Martin
Schmidt, Laura
Hakel, Lukas
Timmermann, Lars
Menzler, Katja
Knake, Susanne
Oehrn, Carina R
author_sort Weber, Immo
collection PubMed
description Whereas the effect of vagal nerve stimulation on emotional states is well established, its effect on cognitive functions is still unclear. Recent rodent studies show that vagal activation enhances reinforcement learning and neuronal dopamine release. The influence of vagal nerve stimulation on reinforcement learning in humans is still unknown. Here, we studied the effect of transcutaneous vagal nerve stimulation on reinforcement learning in eight long-standing seizure-free epilepsy patients, using a well-established forced-choice reward-based paradigm in a cross-sectional, within-subject study design. We investigated vagal nerve stimulation effects on overall accuracy using non-parametric cluster-based permutation tests. Furthermore, we modelled sub-components of the decision process using drift-diffusion modelling. We found higher accuracies in the vagal nerve stimulation condition compared to sham stimulation. Modelling suggests a stimulation-dependent increase in reward sensitivity and shift of accuracy-speed trade-offs towards maximizing rewards. Moreover, vagal nerve stimulation was associated with increased non-decision times suggesting enhanced sensory or attentional processes. No differences of starting bias were detected for both conditions. Accuracies in the extinction phase were higher in later trials of the vagal nerve stimulation condition, suggesting a perseverative effect compared to sham. Together, our results provide first evidence of causal vagal influence on human reinforcement learning and might have clinical implications for the usage of vagal stimulation in learning deficiency.
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spelling pubmed-80668862021-04-28 Trust your gut: vagal nerve stimulation in humans improves reinforcement learning Weber, Immo Niehaus, Hauke Krause, Kristina Molitor, Lena Peper, Martin Schmidt, Laura Hakel, Lukas Timmermann, Lars Menzler, Katja Knake, Susanne Oehrn, Carina R Brain Commun Original Article Whereas the effect of vagal nerve stimulation on emotional states is well established, its effect on cognitive functions is still unclear. Recent rodent studies show that vagal activation enhances reinforcement learning and neuronal dopamine release. The influence of vagal nerve stimulation on reinforcement learning in humans is still unknown. Here, we studied the effect of transcutaneous vagal nerve stimulation on reinforcement learning in eight long-standing seizure-free epilepsy patients, using a well-established forced-choice reward-based paradigm in a cross-sectional, within-subject study design. We investigated vagal nerve stimulation effects on overall accuracy using non-parametric cluster-based permutation tests. Furthermore, we modelled sub-components of the decision process using drift-diffusion modelling. We found higher accuracies in the vagal nerve stimulation condition compared to sham stimulation. Modelling suggests a stimulation-dependent increase in reward sensitivity and shift of accuracy-speed trade-offs towards maximizing rewards. Moreover, vagal nerve stimulation was associated with increased non-decision times suggesting enhanced sensory or attentional processes. No differences of starting bias were detected for both conditions. Accuracies in the extinction phase were higher in later trials of the vagal nerve stimulation condition, suggesting a perseverative effect compared to sham. Together, our results provide first evidence of causal vagal influence on human reinforcement learning and might have clinical implications for the usage of vagal stimulation in learning deficiency. Oxford University Press 2021-03-14 /pmc/articles/PMC8066886/ /pubmed/33928247 http://dx.doi.org/10.1093/braincomms/fcab039 Text en © The Author(s) (2021). Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Weber, Immo
Niehaus, Hauke
Krause, Kristina
Molitor, Lena
Peper, Martin
Schmidt, Laura
Hakel, Lukas
Timmermann, Lars
Menzler, Katja
Knake, Susanne
Oehrn, Carina R
Trust your gut: vagal nerve stimulation in humans improves reinforcement learning
title Trust your gut: vagal nerve stimulation in humans improves reinforcement learning
title_full Trust your gut: vagal nerve stimulation in humans improves reinforcement learning
title_fullStr Trust your gut: vagal nerve stimulation in humans improves reinforcement learning
title_full_unstemmed Trust your gut: vagal nerve stimulation in humans improves reinforcement learning
title_short Trust your gut: vagal nerve stimulation in humans improves reinforcement learning
title_sort trust your gut: vagal nerve stimulation in humans improves reinforcement learning
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8066886/
https://www.ncbi.nlm.nih.gov/pubmed/33928247
http://dx.doi.org/10.1093/braincomms/fcab039
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