Learning of new associations invokes a major change in modulations of cortical beta oscillations in human adults
Large‐scale cortical beta (β) oscillations were implicated in the learning processes, but their exact role is debated. We used MEG to explore the dynamics of movement‐related β‐oscillations while 22 adults learned, through trial and error, novel associations between four auditory pseudowords and mov...
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Published in | Psychophysiology Vol. 60; no. 8; pp. e14284 - n/a |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Blackwell Publishing Ltd
01.08.2023
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Subjects | |
Online Access | Get full text |
ISSN | 0048-5772 1469-8986 1469-8986 1540-5958 |
DOI | 10.1111/psyp.14284 |
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Abstract | Large‐scale cortical beta (β) oscillations were implicated in the learning processes, but their exact role is debated. We used MEG to explore the dynamics of movement‐related β‐oscillations while 22 adults learned, through trial and error, novel associations between four auditory pseudowords and movements of four limbs. As learning proceeded, spatial–temporal characteristics of β‐oscillations accompanying cue‐triggered movements underwent a major transition. Early in learning, widespread suppression of β‐power occurred long before movement initiation and sustained throughout the whole behavioral trial. When learning advanced and performance reached asymptote, β‐suppression after the initiation of correct motor response was replaced by a rise in β‐power mainly in the prefrontal and medial temporal regions of the left hemisphere. This post‐decision β‐power predicted trial‐by‐trial response times (RT) at both stages of learning (before and after the rules become familiar), but with different signs of interaction. When a subject just started to acquire associative rules and gradually improved task performance, a decrease in RT correlated with the increase in the post‐decision β‐band power. When the participants implemented the already acquired rules, faster (more confident) responses were associated with the weaker post‐decision β‐band synchronization. Our findings suggest that maximal beta activity is pertinent to a distinct stage of learning and may serve to strengthen the newly learned association in a distributed memory network.
We showed that early and advanced stages of auditory‐motor learning are accompanied by dramatically different states of β‐band neural oscillations: suppression in the beginning and strong synchronization later at learning. Notably, at the advanced stage of learning, the β‐synchronization is weaker after faster (more confident) motor responses, which suggests that maximal beta activity is pertinent to a stage of learning when newly learned associations are being strengthened in a memory network. |
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AbstractList | Large-scale cortical beta (β) oscillations were implicated in the learning processes, but their exact role is debated. We used MEG to explore the dynamics of movement-related β-oscillations while 22 adults learned, through trial and error, novel associations between four auditory pseudowords and movements of four limbs. As learning proceeded, spatial-temporal characteristics of β-oscillations accompanying cue-triggered movements underwent a major transition. Early in learning, widespread suppression of β-power occurred long before movement initiation and sustained throughout the whole behavioral trial. When learning advanced and performance reached asymptote, β-suppression after the initiation of correct motor response was replaced by a rise in β-power mainly in the prefrontal and medial temporal regions of the left hemisphere. This post-decision β-power predicted trial-by-trial response times (RT) at both stages of learning (before and after the rules become familiar), but with different signs of interaction. When a subject just started to acquire associative rules and gradually improved task performance, a decrease in RT correlated with the increase in the post-decision β-band power. When the participants implemented the already acquired rules, faster (more confident) responses were associated with the weaker post-decision β-band synchronization. Our findings suggest that maximal beta activity is pertinent to a distinct stage of learning and may serve to strengthen the newly learned association in a distributed memory network.Large-scale cortical beta (β) oscillations were implicated in the learning processes, but their exact role is debated. We used MEG to explore the dynamics of movement-related β-oscillations while 22 adults learned, through trial and error, novel associations between four auditory pseudowords and movements of four limbs. As learning proceeded, spatial-temporal characteristics of β-oscillations accompanying cue-triggered movements underwent a major transition. Early in learning, widespread suppression of β-power occurred long before movement initiation and sustained throughout the whole behavioral trial. When learning advanced and performance reached asymptote, β-suppression after the initiation of correct motor response was replaced by a rise in β-power mainly in the prefrontal and medial temporal regions of the left hemisphere. This post-decision β-power predicted trial-by-trial response times (RT) at both stages of learning (before and after the rules become familiar), but with different signs of interaction. When a subject just started to acquire associative rules and gradually improved task performance, a decrease in RT correlated with the increase in the post-decision β-band power. When the participants implemented the already acquired rules, faster (more confident) responses were associated with the weaker post-decision β-band synchronization. Our findings suggest that maximal beta activity is pertinent to a distinct stage of learning and may serve to strengthen the newly learned association in a distributed memory network. Large‐scale cortical beta (β) oscillations were implicated in the learning processes, but their exact role is debated. We used MEG to explore the dynamics of movement‐related β‐oscillations while 22 adults learned, through trial and error, novel associations between four auditory pseudowords and movements of four limbs. As learning proceeded, spatial–temporal characteristics of β‐oscillations accompanying cue‐triggered movements underwent a major transition. Early in learning, widespread suppression of β‐power occurred long before movement initiation and sustained throughout the whole behavioral trial. When learning advanced and performance reached asymptote, β‐suppression after the initiation of correct motor response was replaced by a rise in β‐power mainly in the prefrontal and medial temporal regions of the left hemisphere. This post‐decision β‐power predicted trial‐by‐trial response times (RT) at both stages of learning (before and after the rules become familiar), but with different signs of interaction. When a subject just started to acquire associative rules and gradually improved task performance, a decrease in RT correlated with the increase in the post‐decision β‐band power. When the participants implemented the already acquired rules, faster (more confident) responses were associated with the weaker post‐decision β‐band synchronization. Our findings suggest that maximal beta activity is pertinent to a distinct stage of learning and may serve to strengthen the newly learned association in a distributed memory network. Large‐scale cortical beta (β) oscillations were implicated in the learning processes, but their exact role is debated. We used MEG to explore the dynamics of movement‐related β‐oscillations while 22 adults learned, through trial and error, novel associations between four auditory pseudowords and movements of four limbs. As learning proceeded, spatial–temporal characteristics of β‐oscillations accompanying cue‐triggered movements underwent a major transition. Early in learning, widespread suppression of β‐power occurred long before movement initiation and sustained throughout the whole behavioral trial. When learning advanced and performance reached asymptote, β‐suppression after the initiation of correct motor response was replaced by a rise in β‐power mainly in the prefrontal and medial temporal regions of the left hemisphere. This post‐decision β‐power predicted trial‐by‐trial response times (RT) at both stages of learning (before and after the rules become familiar), but with different signs of interaction. When a subject just started to acquire associative rules and gradually improved task performance, a decrease in RT correlated with the increase in the post‐decision β‐band power. When the participants implemented the already acquired rules, faster (more confident) responses were associated with the weaker post‐decision β‐band synchronization. Our findings suggest that maximal beta activity is pertinent to a distinct stage of learning and may serve to strengthen the newly learned association in a distributed memory network. We showed that early and advanced stages of auditory‐motor learning are accompanied by dramatically different states of β‐band neural oscillations: suppression in the beginning and strong synchronization later at learning. Notably, at the advanced stage of learning, the β‐synchronization is weaker after faster (more confident) motor responses, which suggests that maximal beta activity is pertinent to a stage of learning when newly learned associations are being strengthened in a memory network. |
Author | Tretyakova, Vera Prokofyev, Andrey Skavronskaya, Valeriya Nikolaeva, Anastasia Tyulenev, Nikita Pavlova, Anna Stroganova, Tatiana Chernyshev, Boris |
Author_xml | – sequence: 1 givenname: Anna orcidid: 0000-0003-4072-3169 surname: Pavlova fullname: Pavlova, Anna email: anne.al.pavlova@gmail.com organization: HSE University – sequence: 2 givenname: Nikita surname: Tyulenev fullname: Tyulenev, Nikita organization: Moscow State University of Psychology and Education – sequence: 3 givenname: Vera surname: Tretyakova fullname: Tretyakova, Vera organization: Moscow State University of Psychology and Education – sequence: 4 givenname: Valeriya surname: Skavronskaya fullname: Skavronskaya, Valeriya organization: Moscow State University of Psychology and Education – sequence: 5 givenname: Anastasia surname: Nikolaeva fullname: Nikolaeva, Anastasia organization: Moscow State University of Psychology and Education – sequence: 6 givenname: Andrey surname: Prokofyev fullname: Prokofyev, Andrey organization: Moscow State University of Psychology and Education – sequence: 7 givenname: Tatiana surname: Stroganova fullname: Stroganova, Tatiana organization: Moscow State University of Psychology and Education – sequence: 8 givenname: Boris orcidid: 0000-0002-8267-3916 surname: Chernyshev fullname: Chernyshev, Boris organization: Lomonosov Moscow State University |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36906906$$D View this record in MEDLINE/PubMed |
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Keywords | time-frequency analyses action words post-movement β synchronization associative learning rule acquisition magnetoencephalography |
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Snippet | Large‐scale cortical beta (β) oscillations were implicated in the learning processes, but their exact role is debated. We used MEG to explore the dynamics of... Large-scale cortical beta (β) oscillations were implicated in the learning processes, but their exact role is debated. We used MEG to explore the dynamics of... |
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SubjectTerms | action words Adult associative learning Beta Rhythm - physiology Cognition Hemispheric laterality Humans Learning - physiology Magnetoencephalography Movement - physiology Oscillations post‐movement β synchronization Reaction Time - physiology rule acquisition Spatial discrimination learning Synchronization Temporal Lobe time‐frequency analyses |
Title | Learning of new associations invokes a major change in modulations of cortical beta oscillations in human adults |
URI | https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fpsyp.14284 https://www.ncbi.nlm.nih.gov/pubmed/36906906 https://www.proquest.com/docview/2830560690 https://www.proquest.com/docview/2786100807 |
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