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Sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self‐initiated stimuli

Actions modulate sensory processing by attenuating responses to self‐ compared to externally generated inputs, which is traditionally attributed to stimulus‐specific motor predictions. Yet, suppression has been also found for stimuli merely coinciding with actions, pointing to unspecific processes t...

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Autores principales: Paraskevoudi, Nadia, SanMiguel, Iria
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10078310/
https://www.ncbi.nlm.nih.gov/pubmed/35918912
http://dx.doi.org/10.1111/psyp.14156
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author Paraskevoudi, Nadia
SanMiguel, Iria
author_facet Paraskevoudi, Nadia
SanMiguel, Iria
author_sort Paraskevoudi, Nadia
collection PubMed
description Actions modulate sensory processing by attenuating responses to self‐ compared to externally generated inputs, which is traditionally attributed to stimulus‐specific motor predictions. Yet, suppression has been also found for stimuli merely coinciding with actions, pointing to unspecific processes that may be driven by neuromodulatory systems. Meanwhile, the differential processing for self‐generated stimuli raises the possibility of producing effects also on memory for these stimuli; however, evidence remains mixed as to the direction of the effects. Here, we assessed the effects of actions on sensory processing and memory encoding of concomitant, but unpredictable sounds, using a combination of self‐generation and memory recognition task concurrently with EEG and pupil recordings. At encoding, subjects performed button presses that half of the time generated a sound (motor‐auditory; MA) and listened to passively presented sounds (auditory‐only; A). At retrieval, two sounds were presented and participants had to respond which one was present before. We measured memory bias and memory performance by having sequences where either both or only one of the test sounds were presented at encoding, respectively. Results showed worse memory performance – but no differences in memory bias –, attenuated responses, and larger pupil diameter for MA compared to A sounds. Critically, the larger the sensory attenuation and pupil diameter, the worse the memory performance for MA sounds. Nevertheless, sensory attenuation did not correlate with pupil dilation. Collectively, our findings suggest that sensory attenuation and neuromodulatory processes coexist during actions, and both relate to disrupted memory for concurrent, albeit unpredictable sounds.
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spelling pubmed-100783102023-04-07 Sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self‐initiated stimuli Paraskevoudi, Nadia SanMiguel, Iria Psychophysiology Original Articles Actions modulate sensory processing by attenuating responses to self‐ compared to externally generated inputs, which is traditionally attributed to stimulus‐specific motor predictions. Yet, suppression has been also found for stimuli merely coinciding with actions, pointing to unspecific processes that may be driven by neuromodulatory systems. Meanwhile, the differential processing for self‐generated stimuli raises the possibility of producing effects also on memory for these stimuli; however, evidence remains mixed as to the direction of the effects. Here, we assessed the effects of actions on sensory processing and memory encoding of concomitant, but unpredictable sounds, using a combination of self‐generation and memory recognition task concurrently with EEG and pupil recordings. At encoding, subjects performed button presses that half of the time generated a sound (motor‐auditory; MA) and listened to passively presented sounds (auditory‐only; A). At retrieval, two sounds were presented and participants had to respond which one was present before. We measured memory bias and memory performance by having sequences where either both or only one of the test sounds were presented at encoding, respectively. Results showed worse memory performance – but no differences in memory bias –, attenuated responses, and larger pupil diameter for MA compared to A sounds. Critically, the larger the sensory attenuation and pupil diameter, the worse the memory performance for MA sounds. Nevertheless, sensory attenuation did not correlate with pupil dilation. Collectively, our findings suggest that sensory attenuation and neuromodulatory processes coexist during actions, and both relate to disrupted memory for concurrent, albeit unpredictable sounds. John Wiley and Sons Inc. 2022-08-02 2023-01 /pmc/articles/PMC10078310/ /pubmed/35918912 http://dx.doi.org/10.1111/psyp.14156 Text en © 2022 The Authors. Psychophysiology published by Wiley Periodicals LLC on behalf of Society for Psychophysiological Research. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Original Articles
Paraskevoudi, Nadia
SanMiguel, Iria
Sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self‐initiated stimuli
title Sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self‐initiated stimuli
title_full Sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self‐initiated stimuli
title_fullStr Sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self‐initiated stimuli
title_full_unstemmed Sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self‐initiated stimuli
title_short Sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self‐initiated stimuli
title_sort sensory suppression and increased neuromodulation during actions disrupt memory encoding of unpredictable self‐initiated stimuli
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10078310/
https://www.ncbi.nlm.nih.gov/pubmed/35918912
http://dx.doi.org/10.1111/psyp.14156
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