Cargando…

Neural ensembles in the murine medial prefrontal cortex process distinct information during visual perceptual learning

BACKGROUND: Perceptual learning refers to an augmentation of an organism’s ability to respond to external stimuli, which has been described in most sensory modalities. Visual perceptual learning (VPL) is a manifestation of plasticity in visual information processing that occurs in the adult brain, a...

Descripción completa

Detalles Bibliográficos
Autores principales: Wang, Zhenni, Lou, Shihao, Ma, Xiao, Guo, Hui, Liu, Yan, Chen, Wenjing, Lin, Dating, Yang, Yupeng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9960446/
https://www.ncbi.nlm.nih.gov/pubmed/36829186
http://dx.doi.org/10.1186/s12915-023-01529-x
_version_ 1784895516046262272
author Wang, Zhenni
Lou, Shihao
Ma, Xiao
Guo, Hui
Liu, Yan
Chen, Wenjing
Lin, Dating
Yang, Yupeng
author_facet Wang, Zhenni
Lou, Shihao
Ma, Xiao
Guo, Hui
Liu, Yan
Chen, Wenjing
Lin, Dating
Yang, Yupeng
author_sort Wang, Zhenni
collection PubMed
description BACKGROUND: Perceptual learning refers to an augmentation of an organism’s ability to respond to external stimuli, which has been described in most sensory modalities. Visual perceptual learning (VPL) is a manifestation of plasticity in visual information processing that occurs in the adult brain, and can be used to ameliorate the ability of patients with visual defects mainly based on an improvement of detection or discrimination of features in visual tasks. While some brain regions such as the primary visual cortex have been described to participate in VPL, the way more general high-level cognitive brain areas are involved in this process remains unclear. Here, we showed that the medial prefrontal cortex (mPFC) was essential for both the training and maintenance processes of VPL in mouse models. RESULTS: We built a new VPL model in a custom-designed training chamber to enable the utilization of miniScopes when mice freely executed the VPL task. We found that pyramidal neurons in the mPFC participate in both the training process and maintenance of VPL. By recording the calcium activity of mPFC pyramidal neurons while mice freely executed the task, distinct ON and OFF neural ensembles tuned to different behaviors were identified, which might encode different cognitive information. Decoding analysis showed that mouse behaviors could be well predicted using the activity of each ON ensemble. Furthermore, VPL recruited more reward-related components in the mPFC. CONCLUSION: We revealed the neural mechanism underlying vision improvement following VPL and identify distinct ON and OFF neural ensembles in the mPFC that tuned to different information during visual perceptual training. These results uncover an important role of the mPFC in VPL, with more reward-related components being also involved, and pave the way for future clarification of the reward signal coding rules in VPL. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01529-x.
format Online
Article
Text
id pubmed-9960446
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-99604462023-02-26 Neural ensembles in the murine medial prefrontal cortex process distinct information during visual perceptual learning Wang, Zhenni Lou, Shihao Ma, Xiao Guo, Hui Liu, Yan Chen, Wenjing Lin, Dating Yang, Yupeng BMC Biol Research Article BACKGROUND: Perceptual learning refers to an augmentation of an organism’s ability to respond to external stimuli, which has been described in most sensory modalities. Visual perceptual learning (VPL) is a manifestation of plasticity in visual information processing that occurs in the adult brain, and can be used to ameliorate the ability of patients with visual defects mainly based on an improvement of detection or discrimination of features in visual tasks. While some brain regions such as the primary visual cortex have been described to participate in VPL, the way more general high-level cognitive brain areas are involved in this process remains unclear. Here, we showed that the medial prefrontal cortex (mPFC) was essential for both the training and maintenance processes of VPL in mouse models. RESULTS: We built a new VPL model in a custom-designed training chamber to enable the utilization of miniScopes when mice freely executed the VPL task. We found that pyramidal neurons in the mPFC participate in both the training process and maintenance of VPL. By recording the calcium activity of mPFC pyramidal neurons while mice freely executed the task, distinct ON and OFF neural ensembles tuned to different behaviors were identified, which might encode different cognitive information. Decoding analysis showed that mouse behaviors could be well predicted using the activity of each ON ensemble. Furthermore, VPL recruited more reward-related components in the mPFC. CONCLUSION: We revealed the neural mechanism underlying vision improvement following VPL and identify distinct ON and OFF neural ensembles in the mPFC that tuned to different information during visual perceptual training. These results uncover an important role of the mPFC in VPL, with more reward-related components being also involved, and pave the way for future clarification of the reward signal coding rules in VPL. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01529-x. BioMed Central 2023-02-24 /pmc/articles/PMC9960446/ /pubmed/36829186 http://dx.doi.org/10.1186/s12915-023-01529-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Wang, Zhenni
Lou, Shihao
Ma, Xiao
Guo, Hui
Liu, Yan
Chen, Wenjing
Lin, Dating
Yang, Yupeng
Neural ensembles in the murine medial prefrontal cortex process distinct information during visual perceptual learning
title Neural ensembles in the murine medial prefrontal cortex process distinct information during visual perceptual learning
title_full Neural ensembles in the murine medial prefrontal cortex process distinct information during visual perceptual learning
title_fullStr Neural ensembles in the murine medial prefrontal cortex process distinct information during visual perceptual learning
title_full_unstemmed Neural ensembles in the murine medial prefrontal cortex process distinct information during visual perceptual learning
title_short Neural ensembles in the murine medial prefrontal cortex process distinct information during visual perceptual learning
title_sort neural ensembles in the murine medial prefrontal cortex process distinct information during visual perceptual learning
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9960446/
https://www.ncbi.nlm.nih.gov/pubmed/36829186
http://dx.doi.org/10.1186/s12915-023-01529-x
work_keys_str_mv AT wangzhenni neuralensemblesinthemurinemedialprefrontalcortexprocessdistinctinformationduringvisualperceptuallearning
AT loushihao neuralensemblesinthemurinemedialprefrontalcortexprocessdistinctinformationduringvisualperceptuallearning
AT maxiao neuralensemblesinthemurinemedialprefrontalcortexprocessdistinctinformationduringvisualperceptuallearning
AT guohui neuralensemblesinthemurinemedialprefrontalcortexprocessdistinctinformationduringvisualperceptuallearning
AT liuyan neuralensemblesinthemurinemedialprefrontalcortexprocessdistinctinformationduringvisualperceptuallearning
AT chenwenjing neuralensemblesinthemurinemedialprefrontalcortexprocessdistinctinformationduringvisualperceptuallearning
AT lindating neuralensemblesinthemurinemedialprefrontalcortexprocessdistinctinformationduringvisualperceptuallearning
AT yangyupeng neuralensemblesinthemurinemedialprefrontalcortexprocessdistinctinformationduringvisualperceptuallearning