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Multisensory learning binds neurons into a cross-modal memory engram
Associating multiple sensory cues with objects and experience is a fundamental brain process that improves object recognition and memory performance. However, neural mechanisms that bind sensory features during learning and augment memory expression are unknown. Here we demonstrate multisensory appe...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10208976/ https://www.ncbi.nlm.nih.gov/pubmed/37100911 http://dx.doi.org/10.1038/s41586-023-06013-8 |
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author | Okray, Zeynep Jacob, Pedro F. Stern, Ciara Desmond, Kieran Otto, Nils Talbot, Clifford B. Vargas-Gutierrez, Paola Waddell, Scott |
author_facet | Okray, Zeynep Jacob, Pedro F. Stern, Ciara Desmond, Kieran Otto, Nils Talbot, Clifford B. Vargas-Gutierrez, Paola Waddell, Scott |
author_sort | Okray, Zeynep |
collection | PubMed |
description | Associating multiple sensory cues with objects and experience is a fundamental brain process that improves object recognition and memory performance. However, neural mechanisms that bind sensory features during learning and augment memory expression are unknown. Here we demonstrate multisensory appetitive and aversive memory in Drosophila. Combining colours and odours improved memory performance, even when each sensory modality was tested alone. Temporal control of neuronal function revealed visually selective mushroom body Kenyon cells (KCs) to be required for enhancement of both visual and olfactory memory after multisensory training. Voltage imaging in head-fixed flies showed that multisensory learning binds activity between streams of modality-specific KCs so that unimodal sensory input generates a multimodal neuronal response. Binding occurs between regions of the olfactory and visual KC axons, which receive valence-relevant dopaminergic reinforcement, and is propagated downstream. Dopamine locally releases GABAergic inhibition to permit specific microcircuits within KC-spanning serotonergic neurons to function as an excitatory bridge between the previously ‘modality-selective’ KC streams. Cross-modal binding thereby expands the KCs representing the memory engram for each modality into those representing the other. This broadening of the engram improves memory performance after multisensory learning and permits a single sensory feature to retrieve the memory of the multimodal experience. |
format | Online Article Text |
id | pubmed-10208976 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-102089762023-05-26 Multisensory learning binds neurons into a cross-modal memory engram Okray, Zeynep Jacob, Pedro F. Stern, Ciara Desmond, Kieran Otto, Nils Talbot, Clifford B. Vargas-Gutierrez, Paola Waddell, Scott Nature Article Associating multiple sensory cues with objects and experience is a fundamental brain process that improves object recognition and memory performance. However, neural mechanisms that bind sensory features during learning and augment memory expression are unknown. Here we demonstrate multisensory appetitive and aversive memory in Drosophila. Combining colours and odours improved memory performance, even when each sensory modality was tested alone. Temporal control of neuronal function revealed visually selective mushroom body Kenyon cells (KCs) to be required for enhancement of both visual and olfactory memory after multisensory training. Voltage imaging in head-fixed flies showed that multisensory learning binds activity between streams of modality-specific KCs so that unimodal sensory input generates a multimodal neuronal response. Binding occurs between regions of the olfactory and visual KC axons, which receive valence-relevant dopaminergic reinforcement, and is propagated downstream. Dopamine locally releases GABAergic inhibition to permit specific microcircuits within KC-spanning serotonergic neurons to function as an excitatory bridge between the previously ‘modality-selective’ KC streams. Cross-modal binding thereby expands the KCs representing the memory engram for each modality into those representing the other. This broadening of the engram improves memory performance after multisensory learning and permits a single sensory feature to retrieve the memory of the multimodal experience. Nature Publishing Group UK 2023-04-26 2023 /pmc/articles/PMC10208976/ /pubmed/37100911 http://dx.doi.org/10.1038/s41586-023-06013-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Okray, Zeynep Jacob, Pedro F. Stern, Ciara Desmond, Kieran Otto, Nils Talbot, Clifford B. Vargas-Gutierrez, Paola Waddell, Scott Multisensory learning binds neurons into a cross-modal memory engram |
title | Multisensory learning binds neurons into a cross-modal memory engram |
title_full | Multisensory learning binds neurons into a cross-modal memory engram |
title_fullStr | Multisensory learning binds neurons into a cross-modal memory engram |
title_full_unstemmed | Multisensory learning binds neurons into a cross-modal memory engram |
title_short | Multisensory learning binds neurons into a cross-modal memory engram |
title_sort | multisensory learning binds neurons into a cross-modal memory engram |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10208976/ https://www.ncbi.nlm.nih.gov/pubmed/37100911 http://dx.doi.org/10.1038/s41586-023-06013-8 |
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